24
Microalgae for a macroenergy world Suphi S. Oncel n Ege University, Faculty of Engineering, Department of Bioengineering, Izmir 35100, Turkey article info Article history: Received 18 June 2012 Received in revised form 19 May 2013 Accepted 26 May 2013 Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important dilemmas of the modern world is to supply enough energy with minimal environmental impact. On this demand bioenergy from renewable biofuels is of growing public and private interest. Recent developments in the scientic researches show that microalgae have potential as a source of bioenergy. With their exception of being one of the oldest residents of the Earth and playing a vital role in building up the atmosphere, microalgae have a variety of diversied strains, biochemical routes and products that can be used for biofuel processing. An increasing number of researchers, academics, entrepreneurs and investors are now working on new technologies to adapt microalgae originated energy into our daily life. The aim of this review is to focus on microalgae based biofuels under the main titles of biodiesel, biohydrogen, bioethanol and biomethane. For evolution in bioenergy that started with the rst generation way through the third generation and today stepping on the concept of fourth generation, microalgae will be a good candidate for an alternative energy source. & 2013 Elsevier Ltd. All rights reserved. Contents 1. Introduction ........................................................................................................ 241 2. Biofuels from microalgae.............................................................................................. 242 2.1. Biodiesel ..................................................................................................... 242 2.2. Biohydrogen .................................................................................................. 248 2.3. Bioethanol ................................................................................................... 249 2.4. Biomethane .................................................................................................. 252 2.5. Integrated processes ........................................................................................... 252 2.6. Light to fuel .................................................................................................. 255 2.7. Future prospects .............................................................................................. 257 3. Economy .......................................................................................................... 257 4. Ethical issues ....................................................................................................... 259 5. Conclusions ........................................................................................................ 260 References ............................................................................................................. 260 1. Introduction Today main streams of energy consumption can be listed as electricity generation, industrial activities, transportation, com- mercial and residential needs. This energy demand is supplied from resources such as coal, natural gas, nuclear power, liquid fossil fuels and renewables (mainly hydropower). According to the projections, world marketed energy consumption will increase up to 739 quadrillion BTU by the year 2035 which exceeds the value of year 1990 by twofolds [1]. Even with some deviations these projections show the massive energy need for the future, in other words the importance of using each and every energy source. With the approach of the second millennium, concerns about environment related with pollution and global warming started to Contents lists available at ScienceDirect journal homepage: www.elsevier.com/locate/rser Renewable and Sustainable Energy Reviews 1364-0321/$ - see front matter & 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.rser.2013.05.059 n Tel./fax: +90 2323884955. E-mail address: [email protected] Renewable and Sustainable Energy Reviews 26 (2013) 241264

Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

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Page 1: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264

Contents lists available at ScienceDirect

Renewable and Sustainable Energy Reviews

1364-03httpd

n TelE-m

journal homepage wwwelseviercomlocaterser

Microalgae for a macroenergy world

Suphi S Oncel n

Ege University Faculty of Engineering Department of Bioengineering Izmir 35100 Turkey

a r t i c l e i n f o

Article historyReceived 18 June 2012Received in revised form19 May 2013Accepted 26 May 2013Available online 19 June 2013

KeywordsMicroalgaeBiofuelsBiodieselBiohydrogenBioethanolBiomethane

21$ - see front matter amp 2013 Elsevier Ltd Axdoiorg101016jrser201305059

fax +90 2323884955ail address suphioncelegeedutr

a b s t r a c t

One of the most important dilemmas of the modern world is to supply enough energy with minimalenvironmental impact On this demand bioenergy from renewable biofuels is of growing public andprivate interest

Recent developments in the scientific researches show that microalgae have potential as a source ofbioenergy With their exception of being one of the oldest residents of the Earth and playing a vital rolein building up the atmosphere microalgae have a variety of diversified strains biochemical routes andproducts that can be used for biofuel processing An increasing number of researchers academicsentrepreneurs and investors are now working on new technologies to adapt microalgae originatedenergy into our daily life

The aim of this review is to focus on microalgae based biofuels under the main titles of biodieselbiohydrogen bioethanol and biomethane

For evolution in bioenergy that started with the first generation way through the third generationand today stepping on the concept of fourth generation microalgae will be a good candidate for analternative energy source

amp 2013 Elsevier Ltd All rights reserved

Contents

1 Introduction 2412 Biofuels from microalgae 242

21 Biodiesel 24222 Biohydrogen 24823 Bioethanol 24924 Biomethane 25225 Integrated processes 25226 Light to fuel 25527 Future prospects 257

3 Economy 2574 Ethical issues 2595 Conclusions 260References 260

1 Introduction

Today main streams of energy consumption can be listed aselectricity generation industrial activities transportation com-mercial and residential needs This energy demand is supplied

ll rights reserved

from resources such as coal natural gas nuclear power liquidfossil fuels and renewables (mainly hydropower) According to theprojections world marketed energy consumption will increase upto 739 quadrillion BTU by the year 2035 which exceeds the valueof year 1990 by twofolds [1] Even with some deviations theseprojections show the massive energy need for the future in otherwords the importance of using each and every energy source

With the approach of the second millennium concerns aboutenvironment related with pollution and global warming started to

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264242

increase the pressure on the societies On the other hand rapiddeclines in global petroleum reserves and escalating prices havemade it obligatory to move towards the development of alter-native energy sources

In the search of new energy substitutes carbon neutral cost-effective sustainable and environmentally friendly renewablefuels from biological resources have received the main attentionMicroalgae can be a good example for a renewable energy sourcethat holds a potential without an adverse effect on the supply offood and other crop products [2ndash4]

Microalgae are photosynthetic free floating microorganismsthat can form filaments and colonies which have high ability forthe adaptation even to extreme ecological habitats They are ableto convert light and carbon dioxide through cellular activities toproduce special chemicals like carbohydrates proteins lipidsvitamins and pigments [2ndash4] Contemporary commercial micro-algae production depends on these chemicals that have applica-tion in cosmetic health food feed supplement chemical andpharmaceutical industries (Table 1)

Even if the main focus is still on the biochemical products theconcept of using microalgae as a source of fuel is starting to catchattention The know-how from the commercial production con-structs the basis for the progress that encouraged the researchersin the universities and institutes to put more effort into developingthe microalgal energy production systems A good indication ofthis interest can be seen from the academic researches consideringbioenergy frommicroalgae The number of published papers aboutmicroalgae from different countries referenced in Science CitationIndex has a clear acceleration with the turn of the 1990s (Fig 1) Ata first glance the reason of this acceleration can be grounded onthe fact of spread internet use more publishing journals andbetter interaction between researchers all around the globe Onthe other hand in the last decade the increase in the number ofcompanies up to 200 involved in producing fuel from algae is theviable sign of this effort and interaction (Table 2) As can be seenfrom the top 10 countries considering the number of publicationsand companies there is a clear relation (Fig 1) which is importantfor the realization of the scientific developments to leap to thecommercial scale [56]

Today global awareness of the societies has been kept alivewith the bombardment of news about biofuels It became ordinary

Table 1Commercial products from microalgae (OP open ponds PBRs photobioreactors P ph

Microalgae Product Prod

Spirulina platensis Phycocyanin biomass OP PChlorella vulgaris Lipid biomass OP PDunaliella salina Carotenoids β-carotene OP PLyngbya majuscule Immune modulators OP PHaematococcus pluvialis Carotenoids astaxanthin OP PMonodus subterraneus Eicosapentaenoic acid OP POdontella aurita Fucoxanthin fatty acids OPPorphyridium cruentum Polysaccharides PBRsAphanizomenon flosaquae Glycoproteins vitamins lipids OP PIsochrysis galbana Fatty acids OP PPhaedactylum tricornutum Lipids fatty acids OP PEuglena gracilis α-Tocopherol biotin PBRsNitzchia laevis Eicosapentaenoic acid PBRsCrypthecodinium cohnii Docosahexaenoic acid PBRsChlorella protothecoides Biomass lipids tocopherol PBRsGaldieria sulphuraria C-phycocyanin PBRsAphanizomenon flos-aquae Vitamins fatty acids phycocyanin OP PShizochytrium sp Docosahexaenoic acid PBRsChlorella minutissima Eicosapentaenoic acid PBRsPrototheca moriformis Vitamin C PBRsParietochloris incise Arachidonic acid PBRsTetraselmis suecica Lipids PUFA OP PNannochloropsis oculata Lipids OP P

to hear announcements about microalgal biofuels with fancyslogans like saving the world But because not much was donecompared to the talks microalgal biofuels are losing ground Themotivation of this review is to give detailed background about theworks that has been done with microalgae to obtain biofuelswith biochemical pathways through the years and summarizethem according to the biofuel type even in a limited space of areview text

2 Biofuels from microalgae

When processed through chemical or biological reactionsmicroalgae can provide different types of renewable biofuels(Fig 2) These include biodiesel biohydrogen bioethanol andbiomethane With regard to microalgae based fuels the main focusis on the biodiesel production Biohydrogen production is alsopopular with its potential in modern applications like fuel cellsThe other two bioethanol and biomethane are considered as apart of integrated processes

21 Biodiesel

Technically biodiesel is an alternative transportation fuel basedon monoalkyl ester building blocks of long-chain fatty acids that isproduced commercially from some common vegetable sourcesincluding soy sunflower safflower canola and palm [78]

Because of the growing public deprecation about the use offood crops for fuel production researchers have turned their focusto alternative non-food related substitutes such as microalgae [7]

Microalgae can form diverse kinds of cellular lipids includingneutral lipids polar lipids wax esters sterols and hydrocarbonsbesides prenyl derivatives such as tocopherols carotenoids ter-penes quinones and phytylated pyrrole derivatives such as chlor-ophylls [9]

Compared to vegetables these lipids have diversified fatty acidcompositions with higher unsaturation levels The size of the fattyacid chains and their level of unsaturation play an important rolein the quality of the biodiesel High quality biodiesel shouldhave low temperature performance and oxidative stability Thesetwo constraints can be supplied by low concentrations of both

ototrophic H heterotrophic)Source Adapted from Refs [2135ndash138]

uction Mode Application

BRs P Health food cosmeticsBRs PH Health food food supplement feedBRs PH Health food food supplement feedBRs H Pharmaceuticals nutritionBRs PH Health food pharmaceuticals feed additivesBRs P Pharmaceuticals nutrition

P Pharmaceuticals cosmetics baby foodPH Pharmaceuticals cosmetics nutrition

BRs P Pharmaceuticals cosmetics nutrition nuritionBRs PH Animal nutritionBRs PH Pharmaceuticals nutrition

PH Pharmaceuticals nutritionH Pharmaceuticals nutritionH Pharmaceuticals nutritionPH Pharmaceuticals nutritionPH Health food cosmetics

BRs P Pharmaceuticals nutritionH Pharmaceuticals nutritionPH Pharmaceuticals nutritionH Pharmaceuticals nutritionP Pharmaceuticals nutrition

BRs PH Pharmaceuticals nutritionBRs PH Pharmaceuticals cosmetics nutrition

Table 2List of companies working on microalgal biofuel technologiesSource Adapted from Refs [139ndash142]

A2Be Carbon Capture Algae Venture Systems Algaewheel AlgaEnergy

AlgoDyne Ethanol Energy Corp Aquaflow Bionomic Aquatic Energy Aurora Algae IncAlgasol Algenol Amyris Biotech Algaecake Tech CorpAXI Algafuel Algae Biotech SA Algae Link NVAirbus Air New Zealand Boeing BioAlgaene LLCBlue Marble Energy Bodega Algae BBI BionavitasBTR Labs Biofuel Systems Biomara Bisantech Nuova GmbHContinental Airlines Cequesta Algae Carbon Capture Corporation CellanamdashShell amp HR BiopetroleumChevron Culturing Solutions Inc Clean Algae SA Circle Biodiesel amp Ethanol CorporationCommunity Fuels Canadian Pacific Algae Center of Excellence for Hazardous

Materials ManagementDynamic Biogenics

Diversified Energy DFI Group ENEL EADS and IGV GmbHEnhanced Biofuels amp Technologies Fluid Imaging Technologies General Atomics Green Gold Algae and Seaweed Sciences IncGeneral Electric GreenFuel Technologies Corporation Greenshift Green Star Products IncGreenbelt Resources Corporation Global Green Solutions Hawaiian Electric Company HR BiopetroleumInventure Chemical Technology Ingrepo Infinifuel Biodiesel International EnergyImperium Renewables Jet Blue Japan Air KelcoKuehnleAgrosystems Kai Bioenergy KLM Airlines LiveFuelsLS9 Synthetic Bioenergy solutions MBD Biodiesel Neptune Neste OilNorthington Energy Organic Fuels OriginOil Ocean Technology amp Environmental ConsultingOilfox Argentina Petro Algae Phycal Pure Power EnergyPetroSun Biofuels Phyco2 Planktonix Corporation ProvironRenewable Energy Group Revolution Biofuels SeaAg SBAE IndustriesSunx Algae Oil Research Lab Solena Group Sapphire Energy SeambioticSolazyme SunEco Sunrise Ridge Solix BiofuelsSolray Synthetic genomics and Exxon Mobil Corp SGC Energia SGPS SA SAIC CorpTexas Clean Fuels Virgin Airways Valcent VG energyW2 Energy XL RenewablesmdashSigmae

Fig 1 Annual publication count and the top 10 countries considering the number of publications and companiesSource Adapted from Refs [139ndash142198]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 243

long-chain saturated and poly-unsaturated fatty acid oils [10ndash12]Fatty acid profiles of the microalgae depend on the species andculture conditions During optimum culture conditions microalgaesynthesize fatty acids (up to 20 of dry cell weight) mainly for

esterification into glycerol based membrane lipids But when facedwith stress conditions microalgae can diverge from lipid produc-tion pathway towards the synthesis and accumulation of neutrallipids that may reach up to 50 dry cell weight mainly in the form

MIC

RO

ALG

AE

Oil Extraction

Hydrotreatment Green Diesel

Transesterification Biodiesel

Fermentation

Ethanol

Hydrogen

Gasification Syngas

Fermentation

Ethanol

Butanol

Butyric Acid

Acetic Acid

Methane

Methanetion Methane

Hydrogen

Anaerobic Digestion Methane

Biophotolysis Hydrogen

Pyrolysis

Bio-oil

Syngas

Charcoal

Fig 2 Biofuel routes from the standpoint of microalgaeSource Adapted from Refs [816108199]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264244

of triacylglycerols which are actually the key component of algallipids for biodiesel production Triacylglycerols are distinct frommembrane glycerolipids because of their character as the storagematerial for energy instead of structural usage [913]

Lipid productivity of a microalga is accepted to be an indicatorof its potential for biodiesel production

Studies focus on different parameters such as nutrient sourcenutrient concentration light intensity salinity pH mixing speed andtemperature to enhance the lipid productivity of the microalgae(Table 3) Microalgae show variable responses to the effects resultingin various lipid productivities For example on cultivation with 10CO2 biomass productivity of the Scenedesmus sp was higher thanBotryococcus branuii on the other hand lipid productivity was lowerbut similar productivities could be seen in the case of flue gas(55 CO2) cultivation [14] In another study results indicated thatpotassium phosphate and magnesium sulfate are the major mediacomponents affecting the lipid productivity of Botryococcus branuiiand the lipid and biomass optimized media should differ in concen-trations [15] The key is to select the proper method of approachconsidering the microalga for the lipid productivity

Extraction of microalgal lipids is the bottleneck for high yield inproductions After the harvest the culture starts its downstreamjourney As a first step the excess water that is an unwantedvolumetric load is removed through concentration processes likefiltration drying flocculation and centrifugation The concentratedcells can either be extracted directly or through a disruption stepin which the intercellular content was released to enhance theextraction process Considering microalgae because the targetproduct oil is trapped inside strong cell walls the disruption stepcan be termed as a part of the extraction step [16ndash18] Microalgaloils could be extracted using milling expeller press high pressurehomogenization solvent enzyme supercritical fluid osmoticshock pulsed electric field microwave or ultrasound techniquesThe selection of the method depends on the specie cost andefficiency as well as the environmental concerns The extractedlipids then passed to the fractionation step where the undesiredpolar lipids and non-acylglycerol neutral lipids (such as free fattyacids hydrocarbons sterols ketones carotenes and chlorophylls)were removed Later the purified product is converted intobiodiesel through the transesterification process [19ndash24]

Table 3Various studies focusing on lipid productivities as the key element for biodiesel production

Microalgae Effect Time Cultivation PBR type Lightintensity(lE mminus2 sminus1)

Temp(1C)

Medium Maximum production Ref

Botryococcus braunii(UTEX 572)

CO2 14 days Batchndashautotrophic Bubble column 150 2571 Modified Chu 13 5517153 mg Lminus1 dminus1 (21 biomass) with10 CO2 enriched air

2065 mg Lminus1 dminus1 (24) with 55 CO2

containing flue gas

[14]

Botryococcus braunii(765)

CO2 28 days Batchndashautotrophic Airlift (3 L) 150710 25 Modified BG11 1174 mg Lminus1dminus1 (12717083 biomass) with20 CO2 enriched air

[143]

Botryococcus braunii(UTEX 572)

Media components 18 days Batchndashautotrophic Bubble column(06 L)

50 22 Modified BG11 019 g Lminus1 dminus1 (6496 biomass) in lipidoptimized media

018 g Lminus1 dminus1 (5956 biomass) in growthoptimized media

[15]

Botryococcus braunii(KMITL 2)

Light intensity light cycle nitrogenphosphorus iron cultivation time salinity

40 days Batchndashautotrophic Flasks (1 L) 0ndash538(LD cycle)

25 Chlorella 54697313 with 200 mE mminus2 sminus1 continuouslight 222 mg Lminus1 phosphorus and a salinity of0 psu

[144]

Chlamydomonasreinhardtii

pH and CO2 31 days Batchndashautotrophic BIOCOIL (15 L) 220 2571 Artificial or wastewater

05057002 g Lminus1 dminus1 (2525 biomass) with 33CO2 at pH 75

[145]

Chlorella vulgaris(CCAP 211)

Temperature nitrogen concentration andextraction techniques

14 day Batchndashautotrophic Erlenmayer flask(2 L)

70 15ndash25 Guillard F2 20227060 mg Lminus1 dminus1 (14717030) at25 1C

20307040 mg Lminus1 dminus1 (15317051) with0375 g Lminus1 nitrogen concentration

[146]

Chlorella sorokiniana(GXNN01)

Carbon sources and concentrations 70 h Batchndashautotrophicheterotrophic

Erlenmayer flask(015 L)

0ndash80 3072 BBM 028870008 g Lminus1 (028770018 g gDWminus1)with acetate

Glucose concentration of 20 mmol Lminus1 gavethe maximal lipid yield

0048 lipid gminus1DW dayminus1 (232) inmixotrophic perfusion (rate 28 L hminus1)culture

[147]

Chlorella minutisima(UTEX LB-2341)

Long term outdoor production 80 days Batch or perfusionautotrophicndashmixotrophic

Cylindrical vessel(20 L10 200 Ltotal)

0ndash700 30ndash35 Enriched sea water [148]

Chlorellaprotothecoides(UTEX 249)

Carbon source concentration nitrogenconcentration salinity pH level andagitation speed

103 h Batchndashautotrophicmixotrophicheterotrophic

Erlenmeyer flasks(01 L)

8W 26 Modified basal 025 g Lminus1 dminus1 (25257007) with 15 g Lminus1

glucose 69 pH 019 g Lminus1 dminus1 (20337513) with 204 gLminus1

glycerol 71 pH 0177001 g Lminus1 dminus1 (23087318) with

205 g Lminus1 acetate 67 pH

[149]

Chlorellaprotothecoides(SAG 3380)

CO2 14ndash15days

Batchndashautotrophicmixotrophic

Erlenmeyer flasks(025 L)

100710 2471 BG11 with Peptone 213725 DW (Mixotrophic 1 glycerol) 115731 DW (Autotrophic) 358715 DW (Mixotrophic N-deprived)

[150]

Chlorella pyrenoidosa Waste water 10 days BatchndashMixotrophic Flasks (01 L) 63 25ndash27 Diluted piggery wastewater

(with 1000 mg Lminus1 COD) [151]

Chlorella pyrenoidosaFACHB-9

Waste water 120 h Batchfedbatchndashmixotrophic

Flasks (05 L) 405 (1410LD cycle)

2771 Soybean process wastewater

04 g Lminus1 dminus1 (377934 DW) with fed batchculture

[152]

AuxenochlorellaprotothecoidesUMN280

CO2 waste water 12 days Batchndashmixotrophic Roux bottles(058 L)

60 2572 Waste water (05 L)and BG11 seed culture(008 L)

0182 g Lminus1 (1866 DW) without CO2

0418 g Lminus1 (2082 DW) with 1 CO2

0516 gLminus1 (2058 DW) with 5 CO2

[153]

Chlorella vulgaris KNO3 CO2 and light intensity 250 h Batch 24ndash120 25 Artificial sea water [154]

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ndash264245

Table 3 (continued )

Microalgae Effect Time Cultivation PBR type Lightintensity(lE mminus2 sminus1)

Temp(1C)

Medium Maximum production Ref

Membrane spargedcylindrical vessel(5 L)

40 mg Lminus1 dminus1 (20) at 60 mE mminus2sminus1 lightintensity 1 mM KNO3 concentration 1 CO2

enrichmentChlorellavulgarisKCT-CAG10032

CO2 14 days Batchndashautotrophic Bubble column 150 2571 BG11 6917003 mg Lminus1dminus1 (7 biomass) with 10 CO2

enriched air[14]

Chlorella vulgarisBEIJ-H14

Glucose and urea 665 h Fed batchndashheterotrophic

Stirred tank (600 L) Dark 36ndash37 Glucose enrichedmedium

97 dry weight [155]

Chlorella vulgarisCCALA 256

Nutrient limitation 8 days Batchndashautotrophic Thin layer (150 L) 100ndash960 195ndash33

14 SS 032670010 g Lminus1 dminus1 (306705 DW) [156]

Choricystis minor Temperature dilution rate andpostharvest methods

Continuousndashautotrophic

Stirred tank (4 L) 550 10ndash30 BG 11 82 mg Lminus1 dminus1 (213717) at 25 1C and adilution rate of 0014 hminus1

Lipid content increased up to 595716under postharvest conditions withoutphosphate and nitrate

[157]

Nannochloropsisoculata

Temperature nitrogen concentration andextraction techniques

14 days Batchndashautotrophic Erlenmayer Flask(2 L)

70 25ndash38 BBM 9117030 mg Lminus1 dminus1 (14927082) at15 1C

16417011 mg Lminus1 dminus1 (15867059) with0075 gLminus1 nitrogen concentration

[139]

Nannochloropsisoculata

Temperature nitrogen and yeast extractconcentrations

16 days Batchndashphotomixotrophic

Airlift (2 L) 160ndash270 15ndash35 F2 10ndash15 (50 ppm nitrogen) 20-25 (125 ppm nitrogen) 25ndash30 (15 1C) 20ndash25 (35 1C)

[158]

Haematococcuspluvialis

Continuous light intensity or light cyclesno nitrogen or no aeration on production

14 days Batchndashautotrophic Flask 90 24 BBM 15617146 DW Under normal conditions 34857078 DW Under full medium

continuous light with aeration 32997277 DW Under continuous light

aeration no nitrogen

[159]

Neochlorisoleoabundans(UTEX-1185)

Nitrogen sources and concentrations 7 days Batchndashautotrophic Bubble column(1 L)

360 3072 SE 0133 g Lminus1 dminus1 (38) with 5 mM sodium nitrateas nitrogen source

[160]

Neochlorisoleoabundans(UTEX-1185)

Temperature CO2 and nitrate 18 days Batchndashautotrophic Bubble column(1 L)

150 26ndash30 BM 56 biomass with nitrogen starvation at 30 1Ctemperature without CO2 in air

[161]

Neochlorisoleoabundans(UTEX-1185)

Nitrogen starvation 140 h Continuousndashautotrophic

Flat panel airlift(1 L)

270 25 BBM 126 g mminus3 dminus1 (23) continuous culture withno mineral limitation with nitrate starvation

20657013 mg Lminus1dminus1 (9 biomass) with10 CO2 enriched air

3944 mg Lminus1 dminus1 (18) with 55 CO2

containing flue gas 16ndash18 DW with nitrogen deplete two stage

process 10ndash12 DW with single stage process

[162]

Scenedesmus spKCTC AG20831

CO2 14 days Batchndashautotrophic Bubble column 150 2571 BG11 [14]

Tetraselmis suecica Light and nitrogen concentration 9 days Batchndashautotrophic Stirred tank (20 L) 363ndash1331 2071 Modified F2 [163]

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 247

The preferred route for biodiesel production from oils istransesterification rather than pyrolysis and micro-emulsionbecause of the cost and quality concerns [25] Transesterificationis simply the reaction between triacylglycerols and an acyl-acceptor which can be carboxylic acids (acidolysis) alcohols(alcoholysis) or another ester (interesterification) [2526] Biodie-sel production from microalgal oils through transesterificationprocess has several steps (Fig 3)

The reaction can be chemically (acid or base) or biologically(enzyme) catalytic or non-catalytic (high pressure process) [27ndash29]

Homogeneous (NaOH CH3ONa KOH KOCH3) and heterogeneous(alkaline earth metal oxides zeolite KNO3 loaded on Al2O3 KNO3Al2O3 BaO SrO CaO MgO) base catalysts are conventionally used forbiodiesel production They are more effective with an oil having free

Strain selection

- Determination of cell culture condition

- Optimization of lipid production conditions

- Scale -up

Photobioreactor

LightCO2 Nutrients

Separation amp

Refining

Acid Water

CatalystAlcohol Glycerol

Temperature

Fig 3 Microalgal biodiesel productionSource Adapted from Refs [7 4647199200]

fatty acid concentration up to 2 resulting in high reaction rates(4000 faster) and conversion efficiency under lower operationtemperatures compared to acid catalysts But considering watercontent and acidity of the biodiesel feedstock acid catalysts arepreferred to prevent saponification Even if acid catalysts are effectivewith non-edible oils their limitations like the need for higher amountsof alcohol higher temperatures and pressures slower reaction ratesresult in lower yields Both homogeneous and heterogeneous acidcatalysts (sulfuric acid hydrochloric acid phosphoric acid and sulfo-nated organic acids) are used especially in two step biodiesel produc-tion where in the first step the oil reacts with alcohol by acid catalystsand later reacted with the base catalyst This procedure is preferredwith high free fatty acid concentrated oils where the proceduredecreases the value of the free fatty acids to operational levels [1030]

Water

Biomass Harvesting

- Filtration

- Centrifugation

- Sedimentation

- Flotation

Dryer

Oil Extraction

-Chemical

-Biochemical

-Mechanical

Catalyst

-Chemical

-Biological

Oil

Alcohol

Transesterification

Biodiesel

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264248

Conventional technology of chemical catalysis has some con-straints due to the environmental problems related with soapformation and energy demand due to the downstream processesto recover glycerol and catalysts [262831]

Biological catalysis has some advantages over the chemicalcatalysis including lower energy demand moderate reaction con-ditions lower alcohol to oil ratio easier product recovery and highconversion [3132]

Lipases are the key biocatalysts that are used in biodieselproduction Major producer microorganisms for lipases are Aspergil-lus niger Aspergillus oryzae Bacillus pumilis Burkholderla cepaciaCandida antarctica Candida cylindracea Candida lipolytica Candidaparalipolytica Candida rugosa Chromobacterium viscosum Enterobac-ter aerogenes Eremothecium ashbyii Escherichia coli Geotrichumcandidum Mucor miehei Penicillium cyclopium Penicillium expansumPenicillium restrictum Pseudomonas cepacia Pseudomonas fluorescensPseudomonas fragi Rhizopus arrhizus Rhizopus delemar Rhyzomucormiehei Rhizopus oryzae Saccharomyces cerevisiae and Thermomyceslanuginosus which are also commercially important to meet theneeds of the large scale biodiesel processes [3334]

Main bottlenecks of this process include high cost of enzymelow yield due to inactivation longer reaction time slower reactionrate and the amount of water and organic solvents in the reactionmixture [2532]

The limitations in the biocatalysis are managed via the immo-bilization of the lipases in packed bed reactors to prevent washoutand inactivation [35] using whole cell immobilization [26] ionicliquids in enzyme catalysis [3136] genetic modifications andrecombinant microorganisms to enhance the efficiency and theproduction of the enzyme [26] alternative acyl acceptors [37]stepwise processes [3839] moderate polar solvents [40] non-catalytic methods under supercritical conditions [4142] and highpressure processes to stabilize the enzymes [4344]

From the economical point of view which is also importantchemical catalysis is reported to be cheaper than biologicalcatalysis But the modifications like using immobilized biocatalystsand the enhanced reuse can serve a competitive cost compared tothe chemical catalysts [45]

Numerous approaches are still in progress for the optimizationof the biodiesel production process adaptable to different feedtypes compositions and downstream requirements One of thenovel processes mentioned in recent studies is the ldquoMcgyan Processrdquothat consists of a continuous fixed bed reactor that can producebiodiesel using a metal oxide based catalyst The process is analternative method for continuous transesterification and can use awide variety of feedstock does not consume the catalyst reducesthe reaction time from hours to seconds and does not use water ordangerous chemicals [164647] Treatment of the lipids extractedfrom Dunaliella tertiolecta and Nannochloropsis oculata with Mcgyanprocess to produce biodiesel reached up to 85 in the conversion oftriacylglycerides and free fatty acids to alkyl esters [48]

Alternatively by shifting the production route microalgal oilscan be used to produce ldquogreen dieselrdquo by a process known ascatalytic hydroprocessing The basic difference of this with trans-esterification is the usage of hydrogen rather than the alcohol Alsothe by-products like propane water and carbon dioxide differfrom glycerol of transesterification [816] Green diesel has super-iority over biodiesel with its lower oxygen constitution similar tothe petroleum derived fuels with a near zero oxygen content Theprimary goal of the processes is to produce a minimized oxygencontaining green diesel with maximized final energy content[816] Also because of the high paraffinic hydrocarbon contentgreen diesel has higher cetane numbers and energy content onmass basis compared to biodiesel Using the microalgal oils forgreen diesel will be advantageous because of the applicationpotential in the conventional petroleum refinery systems with

existing infrastructure and the by-products (H2O and CO2) can berecycled to be used in the microalgae cultivation again

With the rapid progress in the area of genetic engineering theresearchers can now present the genome sequences of microalgaefor example a lipid producing microalgae specie that has potentialin biofuel production ie Nannochloropsis gaditana genome isnewly finalized and may become a model organism like Chlamy-domonas reinhardtii Chlorella variabilis Micromonas pusila Ostreo-coccus tauri Ostreococcus lucimarinus Thalassiosira psudonanaEmiliana huxleyii Fragilariopsis cylindrus Aerococcus aophageffe-rens Cyanidioschyzon merolae and Phaeodactylum tricornutum withcompleted genomes [4950] By understanding these model micro-organisms in molecular basis we can have the chance to improveproductivities in future applications

The ultimate idea was the excretion of the oils from themicroalgae cells without the need of extraction step This ideawas supported with the studies focusing on Escherichia coli andSaccharomyces cerevisiae to excrete lipids through membraneswith genetic engineering tools [5152]

22 Biohydrogen

Hydrogen with its unique properties is accepted to be arenewable sustainable and environmentally friendly energy car-rier that serve as one of the most promising alternative solution toovercome the growing environmental concerns considering thefuture energy demands [5354]

Today there are various conventional as well as novel strategiesto produce hydrogen from fossil fuels (steam reforming plasmareforming thermal cracking gasification) biomass (pyrolysismicrobial conversion syngas conversion supercritical conversiongasification) and water (photolysis thermolysis electrolysis)incorporating chemical and biological processes [272955] Evenif the hydrogen production is dominated by the chemical pro-cesses using fossil fuels biological processes started to get moreattention since the first studies in the 1920s [56ndash58]

The metabolic routes for biohydrogen production differ accord-ing to the microorganism [2759]

Microalgae

(a) Direct photolysis 2H2O-light-2H2+O2

(b) Indirect photolysis(1) 12H2O+6CO2-light-C6H12O6+6O2

(2) C6H12O6+12H2O-12H2+6CO2Photosynthetic bacteria(a) Photofermentation CH3COOH+2H2O-light-4H2+2CO2

(b) Water-gas shift CO+H2O-H2+CO2Anaerobic bacteria Dark fermentationC6H12O6+2H2O-4H2+2CO2+2CH3COOH

Related with their photosynthetic productivity and light utili-zation efficiency microalgae can perform special biochemical andphotochemical reactions with minimum requirements that makehydrogen production possible under aerobic and anaerobic envir-onments [60ndash62]

Microalga like Anabaena sp [6364] Chlorella pyrenoidosa [65]Chlorella vulgaris [66] Platymonas subcordiformis [6667] Spirulinaplatensis [68] and especially Chlamydomonas reinhardtii [6970] getattention in biohydrogen production

Microalgae use two classes of oxygen sensitive metalloenzymesnitrogenases and hydrogenases that are closely related with thefinal biohydrogen generation process in photosynthesis [6371]

There are several types of hydrogenases like the hup-encodedNiFe-uptake hydrogenases hox-encoded NiFe-bidirectional hydro-genases FeFe hydrogenases NiFeSe-bidirectional hydrogenases

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 249

and Fe-only hydrogenases utilized by bacteria and microalgae Onthe other hand nitrogenases of purple non-sulfur bacteria andheterocyst microalgae can be classified by their metal cofactor asmolybdenum iron and vanadium types [7273]

Nitrogenase is the part of the biological nitrogen fixation andhydrogenase is capable to catalyze hydrogen consuming reactionsBiohydrogen production based on these enzymes differs in energyconsumption Hydrogenase mediated reactions are about threetimes more efficient than nitrogenase catalyzed reactions based onspent energy in the form of ATP On the other hand nitrogenasesare relatively less sensitive to oxygen compared to hydrogenases[74ndash76] Relatively or not because both enzymes are sensitive tooxygen it is important to control culture conditions for optimalhydrogen production

Microalgal biohydrogen production can take place duringphotosynthesis from water by the two photosystems dark fer-mentation of the reduced carbon produced by photosynthesis andphotofermentation by the enzymatic oxidation of intracellularreductants derived from fermentation [77ndash80]

Even if the studies on microalgal biohydrogen started in the 1930s[568182] it was shown that the production can be achieved by theinactivation of photosynthetic water oxidizing activity catalyzed bythe reaction center of photosystem two (PSII) [83ndash85] the productiv-ities could not reach to meaningful levels until there was a novelprotocol depending on sulfur deprivation [69] This protocol dependson the succession of photosynthetic reactions in which oxygenproduction and carbon accumulation take place and anaerobic photo-reactions through which the consumption of stored photosyntheticcellular metabolites for biohydrogen generation take place Sulfurdeprivation triggers the conversion of PSII centers to an intermediatein the PSII repair cycle in other words from a QB-reducing to aQB-nonreducing form resulting in the decrease of photosyntheticoxygen evolution capacity [86ndash88]

Compared to the other methods like using inhibitors (DBMIBDCMU SAL C1-CCP etc) or alternating lightdark cycle the removalof sulfate from the growth medium achieves a reversible inactiva-tion with sustainable and increased hydrogen production [83ndash85]

Most of the recent studies focused on the two stage sulfurdeprivation protocol however as summarized by some of theexample studies from batch to continuous processes with variousprocedures the use of different microalgae is a good sign of theprogress towards the future (Table 4) But again some microalgaelike Platymonas subcordiformis Platymonas helgolandica or Chla-mydomonas moewusii are not sensitive to sulfur deprivation aswell as Chlamydomonas reinhardtii so utilization of inhibitors andnitrogen starvation enhance the hydrogen production [8990]

Also the outdoor studies point out another bottleneck in theproductions Even if the applications in lab scale are givingpromising results outdoor cultures still cannot reach the compar-able levels Microalgae cells have problems to tolerate the lightinhibition and sulfur deprivation when exposed to direct sunlightoutdoors They need to be acclimated to light before the hydrogenproduction phase [91]

Besides the studies on the enhancement of the biohydrogenproduction focusing on culture techniques like utilization of immobi-lized microalgae or stressed cultivations with regard to light andmedium components the progress in genetic engineering to improveproduction levels focuses on engineering truncated antennas of thespecies for better sunlight utilization outdoors without inhibition orengineering oxygen tolerant species that can produce hydrogen inaerobic conditions which is still under investigation [7392]

23 Bioethanol

Bioethanol may be considered as an alternative clean burningfuel because of its environmentally friendly combustion products

with low greenhouse gas effect relative to fossil fuels Todaycommercial bioethanol production is mainly from agriculturalstocks and raw materials like corn rice wheat cassava sugarcane sugar beet and sweet sorghum through biochemical orthermochemical processes [161793] Even though the route ofproduction depends on the raw material it can be summarized asthe breaking of the biomaterial to simple sugars that furtherfermented using alcohol producing microorganisms The producedethanol later separated and concentrated through downstreamprocesses (Fig 4)

Facing the conflict of global energy and food demand therehave been increasing interest and worldwide studies in producingbioethanol from alternative sources like microalgae rather thanfeedstock that has minor impact in the daily life [161793]

Bioethanol from microalgae can be produced through thefermentation of the microalgal biomass or directly through cellularreactions [9495]

When considering ethanol production via fermentation the keyis the accumulation of starch which is a potential substrate thatcan reach half of the microalgas cellular dry biomass Microalgalstarch can be extracted by mechanical or enzymatic means andfurther separated by downstream processes incorporating wateror an organic solvent This starch will be hydrolyzed to glucose tobe used in ethanol fermentation [9697] Production mainly differsfrom other crop raw materials in the first steps of the processbecause microalgae will need special concentration harvestingand mechanical disruption systems related with their cellularphysiology and culturing [98]

Microalgae can also excrete ethanol directly through the cellwalls by means of intracellular processes under dark becauseillumination prevents the formation of ethanol except for minoramounts This process which is reported in some microalgae likeChlorococcum littorale [99] Chlamydomonas reinhardtii [8384]Chlamydomonas moewusii [100] Chlorella vulgaris [101] Oscilla-toria limnetica [102] Oscillatoria limosa [99] Gleocapsa alpicola[103] Spirulina platensis [68] Cyanoteche sp [99] covers theanaerobic metabolism in algae where the assimilation and forma-tion of hydrogen carbon dioxide formate acetate ethanol lactateglycerol and butannediol take place [1783] Degradation of intracel-lular starch which is the main endogenous carbon source storedduring aerobic phototrophic metabolism to pyruvate is accomplishedby the EmbdenndashMeyerhofndashParnas and pentose phosphate pathwaysusing pyruvate decarboxylase and alcohol dehydrogenase enzymes[99102] As stated by Gfeller and Gibbs [83] the lack of ethanolproduction by the microalgae cells during illumination is related withthe absence of available reduced pyridine nucleotides with theassumption of active acetaldehyde and alcohol dehydrogenases Twopossible conversion routes for acetyl-CoA to acetate and ethanol canbe followed In the former route half of the acetyl-CoA is converted toacetate by a deacylase while the rest is reduced to ethanol withacetaldehyde as intermediate In the latter route acetyl-CoA is reducedto acetaldehyde that undergoes a dismutation sequence until theformation of acetate and ethanol [8384]

Enhancing direct microalgal bioethanol production by geneticmanipulations is also under consideration Genes from the ethanolproducing bacterium Zymomonas mobilis was transfered intomicroalgae Synechococcus sp aiming to give the ability to utilizethe fixed carbon for direct ethanol excretion to the culture volumethrough the cell walls [93104]

The novelty of the process lies in the separation of producedbioethanol from the culture medium This process eliminates theharvesting step that decreases the energy costs and water usageassociated with the separation processes required for algae har-vesting and fuel extraction [94105]

Besides bioethanol being the main product the remainingmicroalgal biomass may be used to produce biomethane again

Table 4Microalgal hydrogen production

Microalgae Cultivation Process PBR type Culture medium Hydrogen productionprocedure

Time H2 production Refs

Anabaena variabilis (CCAP 14034B)

Continuousndashphotoautotrophic

Lab Stirred (300 mL) Nitrogen free Allen-Arnon

Nitrogen free Allen-Arnon medium

Under vacuum for 15 min Increased light intensity for

5 h at the 6th day ofcultivation

35 days 12ndash14 mL gminus1DW hminus1 [164]

Anabaena variabilis (ATCC 29413) Continuousndashphotoautotrophic

Lab Vial (14 mL) Allen-Arnon(containing Na2MoO4 orNa3VO4 or neither)

Under argon flushing 80ndash100 h

Up to 5 nmol hminus1 mg Chlaminus1 at pH levels of 7ndash9 with Na3VO4 added cultures

[165]

Anabaena sp PCC 7120 (3hydrogenase mutants from PCC7120)

Batchndashphotoautotrophic Lab Sealed polystyrenecuvettes (1 cm light path47 mL capacity)

BG 11 Nitrogen free BG 11 medium Under anaerobic conditions Various light intensities

32ndash40 h Up to 08ndash1 mmol per cuvette (47 mL) [63]

Anabaena sp PCC 7120 and itsmutant AMC 414

Continuousndashphotoautotrophic

Outdoor Tubular-coiled (435 L) BG 11 Nitrogen free BG 11 medium Under argon atmosphere Nitrogen free BG 11 medium Under anaerobic conditions Increased light intensity

7 days 149 mL hminus1Lminus1PBR (373 mL total) with themutant

[166]

Anabaena variabilis (ATCC 29413) Batchndashphotoautotrophic Lab Panel (500 mL capacity) BG 11 50 h Up to 40ndash50 mL [167]

Chlamydomonas reinhardtii(CC124)

BatchndashphotomixotrophicSynchronous andunsynchronous growth

Lab Stirred glass bottles(12L)

TAP TAP-S medium (transferred bycentrifugation)

140 h 102 mL (with 4 h synchronizedcultures)

86 mL (with unsynchronized cultures)

[168]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotomixotrophic Lab Stirred glass bottles(500 mL)

TAP TAP-S medium transfer bycentrifugation

TAP-S medium inoculationby TAP culture (10inoculation)

175 mL Lminus1 (with centrifuged cultures under20ndash40 mE mminus2sminus1 average light intensity)

[87]

Chlamydomonas reinhardtii(CC124)

Continuousndashphotomixotrophic

Lab Stirred glass bottles(1050 mL)

TAP-S (90 mmol sulfateadded)

TAP-S medium two stagechemostat with aerobicstage and anaerobic stage

TAP-S medium TAP medium with limiting

sulfate (10ndash20 mM) Anaerobic conditions Sulfur free medium Anaerobic

4000 h Up to 058 mL hminus1Lminus1PBR [169]

Chlamydomonas reinhardtii (Dang137C mt+ and a nonmotilemutant CC 1036 pf18 mt+)

Batchndashphotomixotrophic-immobilized

Lab Panel (160 mL) TAP (046 mM sulfatereplete)

23 days 45 mL dayminus1 (380 mL total) [170]

Chlamydomonas reinhardtii (Dang137C mt+)

Batch-photoautotrophicmixotrophic andheterotrophic

Lab Flat glass bottles PBR(15 L volume)

HS (CO2 bubbling) TAPwith or without CO2

bubbling

60ndash80 h 11704 mmol Lminus1 (sim28 mL (hL)minus1) inphotoautotrophic cultures

45716 mmol Lminus1 (sim40 mL (hL)minus1) inphotoheterotrophic cultures

09708 mmol Lminus1 (sim69 mL (hL)minus1)inphotomixotrophic cultures

[171]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotoautotrophic Lab Flat glass bottles PBR(15 L)

High salt HS sulfur free medium Argon purging during the

first 24 h of deprivation TAP-S medium Various dilutions Anaerobic conditions

100 h 7173 mL Lminus1 (175 mE mminus2sminus1 lightintensity pH 77)

5272 mL Lminus1 (420 mE mminus2sminus1 lightintensity pH 74)

[172]

Chlamydomonas reinhardtii(CC124)

Semi continuousndashphotomixotrophic

Lab Stirred tank (25 L) TAP 127 days 1108 mL [173]

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic-immobilized

Lab Vials (75 mL) TAP TA-S-P (no sulfate nophosphate) medium

Alginate entrapped

160ndash180 h

0307002 mol mminus2 (125 mmol mgminus1 Chl hminus1) [174]

Batchndashphotomixotrophic Lab Glass bottles (325 mL) TAP 192 h 395 mmol106 cellsminus1 hminus1 with TAP-S [90]

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harvested cells flushed withor without argon

Anaerobic conditions TAP-S or TAP-N DCMU mixed ethanol

addition Dark anaerobic

fermentation

Chlamydomonas reinhardtii(CC124)

34 mmol106 cellsminus1 hminus1 with TAP-N

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Stirred tank (1 255 L) TAP-S TAP-S medium transfer bycentrifugation

Various mixing time Various light energy Scale-up

192 h Max with 122 kJ sminus1 mminus3 light energy and25 min mixing time

[202]

1 L PBR 1537005 mL Lminus1 hminus1

25 L PBR 1327005 mL Lminus1 hminus1

5 L PBR 1027005 mL Lminus1 hminus1

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Tubular (110 L) TAP-S TAP-S medium transfer bycentrifugation

Modified with silicananoparticle to enhancescattering

48 h 3121571789 mL (06 mL Lminus1 hminus1) [203]

Chlorella pyrenoidosa C-101 Batchndashphotoautotrophic Lab Bubble column (650 mL) Modified Bristol Nitrogen flushing under dark forldquo420rdquo h

60ndash65 h 6910minus2 m3 kgminus1 cell [65]

Chlorella vulgaris MSU 01 Batchndashphotomixotrophic Lab Stirred (500 mL) Modified BG11 and MJ Anaerobic conditions Corn stalk as carbon source

in the medium

6ndash7 days 26 mL [175]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Dark incubation Anaerobic nitrogen

atmosphere Addition of specific effectors

(DCMU DCCD DBMIBand CCCP)

Continuous illuminationafterwards

8 h 0339 mL hminus1 Lminus1 (144 mL) based on1106 cells mLminus1 at 15 μM CCCP addedculture after 8 h of illumination

[66]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Sulfur deprive medium Incubation under dark Anaerobic conditions Continuous illumination

afterwards

50 h 11720 nL hminus1 (with seawater-S medium) [67]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Torus (15 L) Defined mineral Dark incubation Anaerobic nitrogen

atmosphere 15 μM CCCP addition Continuous illumination

afterwards

4ndash6 days 720 mL hminus1 (2366770 mL) [176]

Platymonas helgolandica vartsingtaoensis

Batchndashphotoautotrophic Lab Jars (130 mL) F2 Anaerobic Illuminated -S medium Dark CCCPDCMU or both

added medium

25 h 0002 mmol Lminus1 withndashS medium 0160 mmol Lminus1 with CCCP medium 0014 mmol Lminus1 with DCMU medium 0290 mmol Lminus1 with CCCP

+DCMU medium

[89]

Spirulina platensis (NIES-46) Batchndashphotoautotrophic Lab Erlenmeyer flasks(60 mL)

SOT Nitrogen free medium Under dark

20 h 2 mmol mgDWminus1 [68]

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Table

4(con

tinu

ed)

Micro

alga

eCu

ltivation

Pro

cess

PBRtype

Culture

med

ium

Hyd

roge

npro

duction

pro

cedure

Time

H2pro

duction

Refs

Anae

robicco

nditions

Syne

chocystissp

PCC68

03an

dits

mutantNDH-1

complex

defi

cien

tM55

Batch

ndashphotoa

utotrop

hicndash

encapsu

lated

Lab

Vials

(2mL)

BG

11

Nitroge

natmosphere

Under

cycled

lightan

ddark

exposure

5day

s0005

ndash004

5mM

[177

]

Tetraspo

rasp

CU25

51Batch

ndashphotom

ixotrophic

Lab

Vials

TAP(w

itho

rwithou

t05mM

β-mercaptoethan

olfor

24h)

Su

lfuran

dnitroge

ndep

rive

dmed

ium

Argon

flush

edan

aerobic

atmosphere

424

h173ndash61

7mm

olmgminus

1Chlahminus1

[178

]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264252

through anaerobic digestion for electricity generation The carbondioxide and discharged water formed as by-products of thefermentation can be recycled for the microalgae cultivation tofulfill the biorefinery concept [94105]

24 Biomethane

Today agricultural plants or by-products are conventionalsources for renewable biogas production which is mainly amixture of methane (55ndash75) and carbon dioxide (25ndash45) byanaerobic digestion Biomethane from the biogas can be used as afuel for transportation and electricity generation or for heatingpurposes especially in the rural areas [16106107]

Microalgae with their dominancy over crop plants by means ofproductivity per hectare triggered the attention for the production ofbiogas The solar energy converted and stored by the microalgae cellsthrough photosynthesis can be transformed into energy through theanaerobic digestion to produce methane [106108]

Microalgal biomass having high cellular lipid starch andprotein low cellulose and on the other hand the absence of ligningives a reliable and effective anaerobic digestion These specifica-tions make microalgae a good alternative for effective biomethaneproduction compared to the other crop plants [16107108]

Microalgal biomass can be processed anaerobically step by stepwith specialized groups of bacteria [109]

Hydrolyzation of biopolymers to monosaccharides by hydro-lytic bacteria

Fermentation of the monosaccharides to carboxylic acids andalcohols by fermentative bacteria

Conversion of the acids and alcohols to acetate hydrogen andcarbon dioxide by acetogenic bacteria

Conversion of the end products of acetogenic reactions tomethane and carbon dioxide by methanogenic bacteria

Microalgal biomass remaining after the anaerobic digestion canbe further processed to make fertilizers that can add an extra valueto the overall process Also the carbon dioxide portion of theproduced biogas can be recycled again to cultivate the neededmicroalgal biomass for processing [107110ndash112]

A predicted model of microalgae biomass for digestion toproduce electrical and thermal energy discussed the economicprofitability related with technical aspects of the productionsystem The results showed that the microalgae productivityharvesting concentration and usage of high rate anaerobic diges-ters are the key factors for the economic energy production [113]

A life cycle perspective study using a stochastic model indi-cated that when compared with the conventional crops likeswitch grass canola and corn the environmental impact ofmicroalgal biomass production is higher with respect to energydemand greenhouse gas emissions and water use regardless ofcultivation location Only in overall land use and eutrophicationpotential microalgae present favorable results [114] This mayseem to be a disadvantage to produce biomethane from microalgalbiomass but the studies also supported that the integratedprocesses using proper photobioreactors combining microalgaecultivation and waste water treatment systems for biomethaneproduction will help to reduce the environmental impacts result-ing in a competitive and effective production [11416115]

25 Integrated processes

Relations between parameters and the target products (bio-mass lipid hydrogen ethanol) are important in the selection ofthe microalgae for efficient biofuel production As can be followedfrom the tables summarizing the microalgal biofuel productions

Sugars

- Sugarcane juice

- Molasses

- Sugar beet

Starch

- Corn

- Oats

- Wheat

- Sago Palm

- Cassava

- Banana wastes

- Rye

- Barley

- Triticale

- Sorghum

- Algal biomass

Lignocellulosic materials

- Crop residues

- Cellulose wastes

- Hardwood

- Harbaceous biomass

- Softwood

- Municipal solid wastes

Fermentation

- Saccharomyces cerevisiae

- Schizosaccharomyces pombe

- Zymomonas mobilis

- Saccharomyces bayanus

- Pichia stipitis

- Candida shehatae

- Pachysolen tannophilus

- Mucor indicus

- Chalara parvispora

- T thermosaccharolyticum

- T Ethanolicus

- B Stearothermophilus

- C thermohydrosulfuricum

- C thermocellum

- Milling

- Grinding

- ShredingBreaking hemicellulose

chains

- Physical

- Chemical

- Physicochemical

- Biological

Hydrolization -Detoxification

-Neutralization

Sugars

- Hexoses

- Pentoses

Separation and

Concentration

- Distillation

- Rectification

- Dehydration

ETHANOL

Fig 4 Ethanol production from biomass productionSource Adapted from Refs [9398201]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 253

studies focus on the separation of production processes into twomain steps growth mediated and product mediated When con-sidering direct biofuel production the main approach is product

mediated for higher lipid hydrogen or ethanol production Whenconsidering biofuel production integrated with other microorgan-isms (Table 5) the main approach is growth mediated for higher

Table 5Integrated biofuel processes working with microalgae

Microalgae System Product Ref

Chlamydomonas reinhardtii (UTEX 90) Enzymatic treatment of algal biomass and conversion to ethanol by Saccharomyces cerevisiae Ethanol [179]Chlamydomonas reinhardtii (UTEX 90) Hydrothermal acid treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [180]Chlorella vulgaris (IAM C-534) Enzymatic treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [181]Synechococcus leopoliensis (IAMM 6) Fermentation of acid treated saccharified algal biomass by yeast Saccharomyces sake (IFO 2347) Ethanol [97]Chlamydomonas reinhardtii Chlorella vulgaris (macroalgae Undaria pinnatifida) Enzymatic treatment of pre-acid hydrolyzed algal biomass fermentation by 4 different strains of Escherichia coli Ethanol [182]Schizocytrium sp Fermentation of hydrothermal treated algal biomass by E coli KO11 Ethanol [183]Microcystis aeruginosa and Anabaena variabilis Hydrolysis and fermentation of Super Critical fluid pretreated algal biomass by Saccharomyces cerevisiae Ethanol [204]Scenedesmus obliquus Fermentation of algal biomass hydrolysate by Kluyveromyces marxianus IGC 2671 Saccharomyces carlsbergensis

ATCC6269 and Saccharomyces bayanusEthanol [205]

Anabaena sp PCC7120 Fermentation of hydrogen produced residual algal biomass by Enterobacter aerogenes Hydrogen [184]Arthrospira (Spirulina) platensis Nannochloropsis sp and Dunaliella tertilecta Anaerobic fermentation of thermal pretreated algal biomass by immobilized Clostridium acetobutylicum Hydrogen acetone

ethanol butanol[206]

Chlorella vulgaris ESP6 Dark fermentation of acid or alkalineenzyme pretreated algal biomass hydrolysate by Clostridium butyricumCGS5

Hydrogen [207]

Chlorella sp Simultaneous hydrolysis and fermentation of algal biomass by sewage sludge consortia Hydrogen [208]Thalassiosira weissflogii Dark fermentation of algal biomass with the thermophilic bacterium Thermotoga neapolitana Hydrogen [209]Chlamydomonas reinhardtii (IAM C-238) Chlorella pyrenoidosa (IAM C-212) andDunaliella tertiolecta (ATCC 30909)

Fermentation of algal biomass by Lactobacillus amylovorous (ATCC 33620) and Rhodobacter sphaeroides RV Hydrogen [185]

Chlamydomonas reinhardtii (IAM C-238) and Dunaliella tertiolecta (ATCC 30909) Fermentation of algal biomass by Lactobacillus amylovorous and Rhodobium marinum (A-501) mixed culture Hydrogen [186]Chlamydomonas (MGA 161) Fermentation of algal biomass by Rhodovulum sulfidophilum (W-1S) Hydrogen [85]Chlamydomonas reinhardtii (C238) Mixed cultivation of Chlamydomonas reinhardtii (C238) with Rhodospirillum rubrum (NCIB 8255) Hydrogen [187]Scnedesmus sp Fermentation of algal biomass by anaerobic digested sludge Hydrogen [188]Arthrospira maxima Anaerobic digestion of algal biomass by sewage sludge consortia Methane [210]Phaeodactylum tricornutum Anaerobic digestion of algal biomass by potato factory origin anaerobic granular sludge Methane [211]Scenedesmus sp Anaerobic digestion of high pressure thermal pretreated raw and residue (from lipid extraction) algal biomass

and by anaerobic digestor sludgeMethane [212]

Scenedesmus sp Anaerobic digestion of ultrasound and thermal pretreated raw algal biomass by sugar factory origin anaerobicgranular sludge

Methane [213]

Scenedesmus sp Anaerobic digestion of mild thermal pretreated raw algal biomass by sugar factory origin anaerobic granularsludge

Methane [214]

Spirulina platensis Anabaena variabilis and Chlorella sp Processing of algal biomass by an integrated system of methanogenic culture and Rhodobacter capsulatus Methane and hydrogen [189]Spirulina platensis (UTEX 1926) Rhodotorula glutinis (2541) Mixed cultivation of microalgae and yeast using waste water Lipid (biodiesel) [190]Spirulina platensis Using excess CO2 from the ethanol fermentation by Saccharomyces cerevisiae Lipid (biodiesel) [119]Botryococcus braunii (two strains BB763 and BB764) Chlorella vulgaris Chlorellapyrenoidosa

Biodiesel production catalyzed by immobilized Penicillium expansum lipase and Candida antarctica lipase B(Novozym 435)

Lipid (biodiesel) [191]

Chlorella vulgaris (21111B) Anaerobic digestion of algal biomass by sewage sludge origin methanogenic culture Methane [112]Chlorella sp and Scenedesmus Anaerobic digestion of algal biomass by sewage sludge culture Methane [106]Chlorella sp Anaerobic digestion of algal biomass by sludge culture Methane [192]Arthrospira platensis Chlamydomonas reinhardtii Chlorella kessleri Dunaliellasalina Euglena gracilis and Scenedesmus obliquus

Anaerobic digestion of algal biomass by sewage sludge culture Methane [107]

Spirulina maxima Anaerobic digestion of algal biomass by sewage sludge culture Methane [193]Chlorella sp and Scenedesmus Anaerobic codigestion of algal biomass with waste paper by methanogenic culture Methane [194]Tetraselmis Anaerobic digestion of algal biomass by methanogenic culture Methane [195]Chlorococcum sp Anaerobic treatment of distillery waste with algal biomass by acidogenicmethanogenic culture Methane [196]Phaeodactylum tricornutum (CCAP10551) Anaerobic digestion of algal biomass by granular seed sludge from digester treating potato processing waste

water dominated by Methanosaeta sp and Methanosarcina spMethane [197]

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 255

biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264256

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

SSOncel

Renew

ableand

SustainableEnergy

Review

s26

(2013)241

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 259

technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

[1] EIA (US Energy Information Administration) International Energy Outlook2010 Washington DC 20585 US 2010 langwwweiagovoiafieoindexhtmlrang

[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264262

[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 2: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264242

increase the pressure on the societies On the other hand rapiddeclines in global petroleum reserves and escalating prices havemade it obligatory to move towards the development of alter-native energy sources

In the search of new energy substitutes carbon neutral cost-effective sustainable and environmentally friendly renewablefuels from biological resources have received the main attentionMicroalgae can be a good example for a renewable energy sourcethat holds a potential without an adverse effect on the supply offood and other crop products [2ndash4]

Microalgae are photosynthetic free floating microorganismsthat can form filaments and colonies which have high ability forthe adaptation even to extreme ecological habitats They are ableto convert light and carbon dioxide through cellular activities toproduce special chemicals like carbohydrates proteins lipidsvitamins and pigments [2ndash4] Contemporary commercial micro-algae production depends on these chemicals that have applica-tion in cosmetic health food feed supplement chemical andpharmaceutical industries (Table 1)

Even if the main focus is still on the biochemical products theconcept of using microalgae as a source of fuel is starting to catchattention The know-how from the commercial production con-structs the basis for the progress that encouraged the researchersin the universities and institutes to put more effort into developingthe microalgal energy production systems A good indication ofthis interest can be seen from the academic researches consideringbioenergy frommicroalgae The number of published papers aboutmicroalgae from different countries referenced in Science CitationIndex has a clear acceleration with the turn of the 1990s (Fig 1) Ata first glance the reason of this acceleration can be grounded onthe fact of spread internet use more publishing journals andbetter interaction between researchers all around the globe Onthe other hand in the last decade the increase in the number ofcompanies up to 200 involved in producing fuel from algae is theviable sign of this effort and interaction (Table 2) As can be seenfrom the top 10 countries considering the number of publicationsand companies there is a clear relation (Fig 1) which is importantfor the realization of the scientific developments to leap to thecommercial scale [56]

Today global awareness of the societies has been kept alivewith the bombardment of news about biofuels It became ordinary

Table 1Commercial products from microalgae (OP open ponds PBRs photobioreactors P ph

Microalgae Product Prod

Spirulina platensis Phycocyanin biomass OP PChlorella vulgaris Lipid biomass OP PDunaliella salina Carotenoids β-carotene OP PLyngbya majuscule Immune modulators OP PHaematococcus pluvialis Carotenoids astaxanthin OP PMonodus subterraneus Eicosapentaenoic acid OP POdontella aurita Fucoxanthin fatty acids OPPorphyridium cruentum Polysaccharides PBRsAphanizomenon flosaquae Glycoproteins vitamins lipids OP PIsochrysis galbana Fatty acids OP PPhaedactylum tricornutum Lipids fatty acids OP PEuglena gracilis α-Tocopherol biotin PBRsNitzchia laevis Eicosapentaenoic acid PBRsCrypthecodinium cohnii Docosahexaenoic acid PBRsChlorella protothecoides Biomass lipids tocopherol PBRsGaldieria sulphuraria C-phycocyanin PBRsAphanizomenon flos-aquae Vitamins fatty acids phycocyanin OP PShizochytrium sp Docosahexaenoic acid PBRsChlorella minutissima Eicosapentaenoic acid PBRsPrototheca moriformis Vitamin C PBRsParietochloris incise Arachidonic acid PBRsTetraselmis suecica Lipids PUFA OP PNannochloropsis oculata Lipids OP P

to hear announcements about microalgal biofuels with fancyslogans like saving the world But because not much was donecompared to the talks microalgal biofuels are losing ground Themotivation of this review is to give detailed background about theworks that has been done with microalgae to obtain biofuelswith biochemical pathways through the years and summarizethem according to the biofuel type even in a limited space of areview text

2 Biofuels from microalgae

When processed through chemical or biological reactionsmicroalgae can provide different types of renewable biofuels(Fig 2) These include biodiesel biohydrogen bioethanol andbiomethane With regard to microalgae based fuels the main focusis on the biodiesel production Biohydrogen production is alsopopular with its potential in modern applications like fuel cellsThe other two bioethanol and biomethane are considered as apart of integrated processes

21 Biodiesel

Technically biodiesel is an alternative transportation fuel basedon monoalkyl ester building blocks of long-chain fatty acids that isproduced commercially from some common vegetable sourcesincluding soy sunflower safflower canola and palm [78]

Because of the growing public deprecation about the use offood crops for fuel production researchers have turned their focusto alternative non-food related substitutes such as microalgae [7]

Microalgae can form diverse kinds of cellular lipids includingneutral lipids polar lipids wax esters sterols and hydrocarbonsbesides prenyl derivatives such as tocopherols carotenoids ter-penes quinones and phytylated pyrrole derivatives such as chlor-ophylls [9]

Compared to vegetables these lipids have diversified fatty acidcompositions with higher unsaturation levels The size of the fattyacid chains and their level of unsaturation play an important rolein the quality of the biodiesel High quality biodiesel shouldhave low temperature performance and oxidative stability Thesetwo constraints can be supplied by low concentrations of both

ototrophic H heterotrophic)Source Adapted from Refs [2135ndash138]

uction Mode Application

BRs P Health food cosmeticsBRs PH Health food food supplement feedBRs PH Health food food supplement feedBRs H Pharmaceuticals nutritionBRs PH Health food pharmaceuticals feed additivesBRs P Pharmaceuticals nutrition

P Pharmaceuticals cosmetics baby foodPH Pharmaceuticals cosmetics nutrition

BRs P Pharmaceuticals cosmetics nutrition nuritionBRs PH Animal nutritionBRs PH Pharmaceuticals nutrition

PH Pharmaceuticals nutritionH Pharmaceuticals nutritionH Pharmaceuticals nutritionPH Pharmaceuticals nutritionPH Health food cosmetics

BRs P Pharmaceuticals nutritionH Pharmaceuticals nutritionPH Pharmaceuticals nutritionH Pharmaceuticals nutritionP Pharmaceuticals nutrition

BRs PH Pharmaceuticals nutritionBRs PH Pharmaceuticals cosmetics nutrition

Table 2List of companies working on microalgal biofuel technologiesSource Adapted from Refs [139ndash142]

A2Be Carbon Capture Algae Venture Systems Algaewheel AlgaEnergy

AlgoDyne Ethanol Energy Corp Aquaflow Bionomic Aquatic Energy Aurora Algae IncAlgasol Algenol Amyris Biotech Algaecake Tech CorpAXI Algafuel Algae Biotech SA Algae Link NVAirbus Air New Zealand Boeing BioAlgaene LLCBlue Marble Energy Bodega Algae BBI BionavitasBTR Labs Biofuel Systems Biomara Bisantech Nuova GmbHContinental Airlines Cequesta Algae Carbon Capture Corporation CellanamdashShell amp HR BiopetroleumChevron Culturing Solutions Inc Clean Algae SA Circle Biodiesel amp Ethanol CorporationCommunity Fuels Canadian Pacific Algae Center of Excellence for Hazardous

Materials ManagementDynamic Biogenics

Diversified Energy DFI Group ENEL EADS and IGV GmbHEnhanced Biofuels amp Technologies Fluid Imaging Technologies General Atomics Green Gold Algae and Seaweed Sciences IncGeneral Electric GreenFuel Technologies Corporation Greenshift Green Star Products IncGreenbelt Resources Corporation Global Green Solutions Hawaiian Electric Company HR BiopetroleumInventure Chemical Technology Ingrepo Infinifuel Biodiesel International EnergyImperium Renewables Jet Blue Japan Air KelcoKuehnleAgrosystems Kai Bioenergy KLM Airlines LiveFuelsLS9 Synthetic Bioenergy solutions MBD Biodiesel Neptune Neste OilNorthington Energy Organic Fuels OriginOil Ocean Technology amp Environmental ConsultingOilfox Argentina Petro Algae Phycal Pure Power EnergyPetroSun Biofuels Phyco2 Planktonix Corporation ProvironRenewable Energy Group Revolution Biofuels SeaAg SBAE IndustriesSunx Algae Oil Research Lab Solena Group Sapphire Energy SeambioticSolazyme SunEco Sunrise Ridge Solix BiofuelsSolray Synthetic genomics and Exxon Mobil Corp SGC Energia SGPS SA SAIC CorpTexas Clean Fuels Virgin Airways Valcent VG energyW2 Energy XL RenewablesmdashSigmae

Fig 1 Annual publication count and the top 10 countries considering the number of publications and companiesSource Adapted from Refs [139ndash142198]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 243

long-chain saturated and poly-unsaturated fatty acid oils [10ndash12]Fatty acid profiles of the microalgae depend on the species andculture conditions During optimum culture conditions microalgaesynthesize fatty acids (up to 20 of dry cell weight) mainly for

esterification into glycerol based membrane lipids But when facedwith stress conditions microalgae can diverge from lipid produc-tion pathway towards the synthesis and accumulation of neutrallipids that may reach up to 50 dry cell weight mainly in the form

MIC

RO

ALG

AE

Oil Extraction

Hydrotreatment Green Diesel

Transesterification Biodiesel

Fermentation

Ethanol

Hydrogen

Gasification Syngas

Fermentation

Ethanol

Butanol

Butyric Acid

Acetic Acid

Methane

Methanetion Methane

Hydrogen

Anaerobic Digestion Methane

Biophotolysis Hydrogen

Pyrolysis

Bio-oil

Syngas

Charcoal

Fig 2 Biofuel routes from the standpoint of microalgaeSource Adapted from Refs [816108199]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264244

of triacylglycerols which are actually the key component of algallipids for biodiesel production Triacylglycerols are distinct frommembrane glycerolipids because of their character as the storagematerial for energy instead of structural usage [913]

Lipid productivity of a microalga is accepted to be an indicatorof its potential for biodiesel production

Studies focus on different parameters such as nutrient sourcenutrient concentration light intensity salinity pH mixing speed andtemperature to enhance the lipid productivity of the microalgae(Table 3) Microalgae show variable responses to the effects resultingin various lipid productivities For example on cultivation with 10CO2 biomass productivity of the Scenedesmus sp was higher thanBotryococcus branuii on the other hand lipid productivity was lowerbut similar productivities could be seen in the case of flue gas(55 CO2) cultivation [14] In another study results indicated thatpotassium phosphate and magnesium sulfate are the major mediacomponents affecting the lipid productivity of Botryococcus branuiiand the lipid and biomass optimized media should differ in concen-trations [15] The key is to select the proper method of approachconsidering the microalga for the lipid productivity

Extraction of microalgal lipids is the bottleneck for high yield inproductions After the harvest the culture starts its downstreamjourney As a first step the excess water that is an unwantedvolumetric load is removed through concentration processes likefiltration drying flocculation and centrifugation The concentratedcells can either be extracted directly or through a disruption stepin which the intercellular content was released to enhance theextraction process Considering microalgae because the targetproduct oil is trapped inside strong cell walls the disruption stepcan be termed as a part of the extraction step [16ndash18] Microalgaloils could be extracted using milling expeller press high pressurehomogenization solvent enzyme supercritical fluid osmoticshock pulsed electric field microwave or ultrasound techniquesThe selection of the method depends on the specie cost andefficiency as well as the environmental concerns The extractedlipids then passed to the fractionation step where the undesiredpolar lipids and non-acylglycerol neutral lipids (such as free fattyacids hydrocarbons sterols ketones carotenes and chlorophylls)were removed Later the purified product is converted intobiodiesel through the transesterification process [19ndash24]

Table 3Various studies focusing on lipid productivities as the key element for biodiesel production

Microalgae Effect Time Cultivation PBR type Lightintensity(lE mminus2 sminus1)

Temp(1C)

Medium Maximum production Ref

Botryococcus braunii(UTEX 572)

CO2 14 days Batchndashautotrophic Bubble column 150 2571 Modified Chu 13 5517153 mg Lminus1 dminus1 (21 biomass) with10 CO2 enriched air

2065 mg Lminus1 dminus1 (24) with 55 CO2

containing flue gas

[14]

Botryococcus braunii(765)

CO2 28 days Batchndashautotrophic Airlift (3 L) 150710 25 Modified BG11 1174 mg Lminus1dminus1 (12717083 biomass) with20 CO2 enriched air

[143]

Botryococcus braunii(UTEX 572)

Media components 18 days Batchndashautotrophic Bubble column(06 L)

50 22 Modified BG11 019 g Lminus1 dminus1 (6496 biomass) in lipidoptimized media

018 g Lminus1 dminus1 (5956 biomass) in growthoptimized media

[15]

Botryococcus braunii(KMITL 2)

Light intensity light cycle nitrogenphosphorus iron cultivation time salinity

40 days Batchndashautotrophic Flasks (1 L) 0ndash538(LD cycle)

25 Chlorella 54697313 with 200 mE mminus2 sminus1 continuouslight 222 mg Lminus1 phosphorus and a salinity of0 psu

[144]

Chlamydomonasreinhardtii

pH and CO2 31 days Batchndashautotrophic BIOCOIL (15 L) 220 2571 Artificial or wastewater

05057002 g Lminus1 dminus1 (2525 biomass) with 33CO2 at pH 75

[145]

Chlorella vulgaris(CCAP 211)

Temperature nitrogen concentration andextraction techniques

14 day Batchndashautotrophic Erlenmayer flask(2 L)

70 15ndash25 Guillard F2 20227060 mg Lminus1 dminus1 (14717030) at25 1C

20307040 mg Lminus1 dminus1 (15317051) with0375 g Lminus1 nitrogen concentration

[146]

Chlorella sorokiniana(GXNN01)

Carbon sources and concentrations 70 h Batchndashautotrophicheterotrophic

Erlenmayer flask(015 L)

0ndash80 3072 BBM 028870008 g Lminus1 (028770018 g gDWminus1)with acetate

Glucose concentration of 20 mmol Lminus1 gavethe maximal lipid yield

0048 lipid gminus1DW dayminus1 (232) inmixotrophic perfusion (rate 28 L hminus1)culture

[147]

Chlorella minutisima(UTEX LB-2341)

Long term outdoor production 80 days Batch or perfusionautotrophicndashmixotrophic

Cylindrical vessel(20 L10 200 Ltotal)

0ndash700 30ndash35 Enriched sea water [148]

Chlorellaprotothecoides(UTEX 249)

Carbon source concentration nitrogenconcentration salinity pH level andagitation speed

103 h Batchndashautotrophicmixotrophicheterotrophic

Erlenmeyer flasks(01 L)

8W 26 Modified basal 025 g Lminus1 dminus1 (25257007) with 15 g Lminus1

glucose 69 pH 019 g Lminus1 dminus1 (20337513) with 204 gLminus1

glycerol 71 pH 0177001 g Lminus1 dminus1 (23087318) with

205 g Lminus1 acetate 67 pH

[149]

Chlorellaprotothecoides(SAG 3380)

CO2 14ndash15days

Batchndashautotrophicmixotrophic

Erlenmeyer flasks(025 L)

100710 2471 BG11 with Peptone 213725 DW (Mixotrophic 1 glycerol) 115731 DW (Autotrophic) 358715 DW (Mixotrophic N-deprived)

[150]

Chlorella pyrenoidosa Waste water 10 days BatchndashMixotrophic Flasks (01 L) 63 25ndash27 Diluted piggery wastewater

(with 1000 mg Lminus1 COD) [151]

Chlorella pyrenoidosaFACHB-9

Waste water 120 h Batchfedbatchndashmixotrophic

Flasks (05 L) 405 (1410LD cycle)

2771 Soybean process wastewater

04 g Lminus1 dminus1 (377934 DW) with fed batchculture

[152]

AuxenochlorellaprotothecoidesUMN280

CO2 waste water 12 days Batchndashmixotrophic Roux bottles(058 L)

60 2572 Waste water (05 L)and BG11 seed culture(008 L)

0182 g Lminus1 (1866 DW) without CO2

0418 g Lminus1 (2082 DW) with 1 CO2

0516 gLminus1 (2058 DW) with 5 CO2

[153]

Chlorella vulgaris KNO3 CO2 and light intensity 250 h Batch 24ndash120 25 Artificial sea water [154]

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ndash264245

Table 3 (continued )

Microalgae Effect Time Cultivation PBR type Lightintensity(lE mminus2 sminus1)

Temp(1C)

Medium Maximum production Ref

Membrane spargedcylindrical vessel(5 L)

40 mg Lminus1 dminus1 (20) at 60 mE mminus2sminus1 lightintensity 1 mM KNO3 concentration 1 CO2

enrichmentChlorellavulgarisKCT-CAG10032

CO2 14 days Batchndashautotrophic Bubble column 150 2571 BG11 6917003 mg Lminus1dminus1 (7 biomass) with 10 CO2

enriched air[14]

Chlorella vulgarisBEIJ-H14

Glucose and urea 665 h Fed batchndashheterotrophic

Stirred tank (600 L) Dark 36ndash37 Glucose enrichedmedium

97 dry weight [155]

Chlorella vulgarisCCALA 256

Nutrient limitation 8 days Batchndashautotrophic Thin layer (150 L) 100ndash960 195ndash33

14 SS 032670010 g Lminus1 dminus1 (306705 DW) [156]

Choricystis minor Temperature dilution rate andpostharvest methods

Continuousndashautotrophic

Stirred tank (4 L) 550 10ndash30 BG 11 82 mg Lminus1 dminus1 (213717) at 25 1C and adilution rate of 0014 hminus1

Lipid content increased up to 595716under postharvest conditions withoutphosphate and nitrate

[157]

Nannochloropsisoculata

Temperature nitrogen concentration andextraction techniques

14 days Batchndashautotrophic Erlenmayer Flask(2 L)

70 25ndash38 BBM 9117030 mg Lminus1 dminus1 (14927082) at15 1C

16417011 mg Lminus1 dminus1 (15867059) with0075 gLminus1 nitrogen concentration

[139]

Nannochloropsisoculata

Temperature nitrogen and yeast extractconcentrations

16 days Batchndashphotomixotrophic

Airlift (2 L) 160ndash270 15ndash35 F2 10ndash15 (50 ppm nitrogen) 20-25 (125 ppm nitrogen) 25ndash30 (15 1C) 20ndash25 (35 1C)

[158]

Haematococcuspluvialis

Continuous light intensity or light cyclesno nitrogen or no aeration on production

14 days Batchndashautotrophic Flask 90 24 BBM 15617146 DW Under normal conditions 34857078 DW Under full medium

continuous light with aeration 32997277 DW Under continuous light

aeration no nitrogen

[159]

Neochlorisoleoabundans(UTEX-1185)

Nitrogen sources and concentrations 7 days Batchndashautotrophic Bubble column(1 L)

360 3072 SE 0133 g Lminus1 dminus1 (38) with 5 mM sodium nitrateas nitrogen source

[160]

Neochlorisoleoabundans(UTEX-1185)

Temperature CO2 and nitrate 18 days Batchndashautotrophic Bubble column(1 L)

150 26ndash30 BM 56 biomass with nitrogen starvation at 30 1Ctemperature without CO2 in air

[161]

Neochlorisoleoabundans(UTEX-1185)

Nitrogen starvation 140 h Continuousndashautotrophic

Flat panel airlift(1 L)

270 25 BBM 126 g mminus3 dminus1 (23) continuous culture withno mineral limitation with nitrate starvation

20657013 mg Lminus1dminus1 (9 biomass) with10 CO2 enriched air

3944 mg Lminus1 dminus1 (18) with 55 CO2

containing flue gas 16ndash18 DW with nitrogen deplete two stage

process 10ndash12 DW with single stage process

[162]

Scenedesmus spKCTC AG20831

CO2 14 days Batchndashautotrophic Bubble column 150 2571 BG11 [14]

Tetraselmis suecica Light and nitrogen concentration 9 days Batchndashautotrophic Stirred tank (20 L) 363ndash1331 2071 Modified F2 [163]

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ndash264246

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 247

The preferred route for biodiesel production from oils istransesterification rather than pyrolysis and micro-emulsionbecause of the cost and quality concerns [25] Transesterificationis simply the reaction between triacylglycerols and an acyl-acceptor which can be carboxylic acids (acidolysis) alcohols(alcoholysis) or another ester (interesterification) [2526] Biodie-sel production from microalgal oils through transesterificationprocess has several steps (Fig 3)

The reaction can be chemically (acid or base) or biologically(enzyme) catalytic or non-catalytic (high pressure process) [27ndash29]

Homogeneous (NaOH CH3ONa KOH KOCH3) and heterogeneous(alkaline earth metal oxides zeolite KNO3 loaded on Al2O3 KNO3Al2O3 BaO SrO CaO MgO) base catalysts are conventionally used forbiodiesel production They are more effective with an oil having free

Strain selection

- Determination of cell culture condition

- Optimization of lipid production conditions

- Scale -up

Photobioreactor

LightCO2 Nutrients

Separation amp

Refining

Acid Water

CatalystAlcohol Glycerol

Temperature

Fig 3 Microalgal biodiesel productionSource Adapted from Refs [7 4647199200]

fatty acid concentration up to 2 resulting in high reaction rates(4000 faster) and conversion efficiency under lower operationtemperatures compared to acid catalysts But considering watercontent and acidity of the biodiesel feedstock acid catalysts arepreferred to prevent saponification Even if acid catalysts are effectivewith non-edible oils their limitations like the need for higher amountsof alcohol higher temperatures and pressures slower reaction ratesresult in lower yields Both homogeneous and heterogeneous acidcatalysts (sulfuric acid hydrochloric acid phosphoric acid and sulfo-nated organic acids) are used especially in two step biodiesel produc-tion where in the first step the oil reacts with alcohol by acid catalystsand later reacted with the base catalyst This procedure is preferredwith high free fatty acid concentrated oils where the proceduredecreases the value of the free fatty acids to operational levels [1030]

Water

Biomass Harvesting

- Filtration

- Centrifugation

- Sedimentation

- Flotation

Dryer

Oil Extraction

-Chemical

-Biochemical

-Mechanical

Catalyst

-Chemical

-Biological

Oil

Alcohol

Transesterification

Biodiesel

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264248

Conventional technology of chemical catalysis has some con-straints due to the environmental problems related with soapformation and energy demand due to the downstream processesto recover glycerol and catalysts [262831]

Biological catalysis has some advantages over the chemicalcatalysis including lower energy demand moderate reaction con-ditions lower alcohol to oil ratio easier product recovery and highconversion [3132]

Lipases are the key biocatalysts that are used in biodieselproduction Major producer microorganisms for lipases are Aspergil-lus niger Aspergillus oryzae Bacillus pumilis Burkholderla cepaciaCandida antarctica Candida cylindracea Candida lipolytica Candidaparalipolytica Candida rugosa Chromobacterium viscosum Enterobac-ter aerogenes Eremothecium ashbyii Escherichia coli Geotrichumcandidum Mucor miehei Penicillium cyclopium Penicillium expansumPenicillium restrictum Pseudomonas cepacia Pseudomonas fluorescensPseudomonas fragi Rhizopus arrhizus Rhizopus delemar Rhyzomucormiehei Rhizopus oryzae Saccharomyces cerevisiae and Thermomyceslanuginosus which are also commercially important to meet theneeds of the large scale biodiesel processes [3334]

Main bottlenecks of this process include high cost of enzymelow yield due to inactivation longer reaction time slower reactionrate and the amount of water and organic solvents in the reactionmixture [2532]

The limitations in the biocatalysis are managed via the immo-bilization of the lipases in packed bed reactors to prevent washoutand inactivation [35] using whole cell immobilization [26] ionicliquids in enzyme catalysis [3136] genetic modifications andrecombinant microorganisms to enhance the efficiency and theproduction of the enzyme [26] alternative acyl acceptors [37]stepwise processes [3839] moderate polar solvents [40] non-catalytic methods under supercritical conditions [4142] and highpressure processes to stabilize the enzymes [4344]

From the economical point of view which is also importantchemical catalysis is reported to be cheaper than biologicalcatalysis But the modifications like using immobilized biocatalystsand the enhanced reuse can serve a competitive cost compared tothe chemical catalysts [45]

Numerous approaches are still in progress for the optimizationof the biodiesel production process adaptable to different feedtypes compositions and downstream requirements One of thenovel processes mentioned in recent studies is the ldquoMcgyan Processrdquothat consists of a continuous fixed bed reactor that can producebiodiesel using a metal oxide based catalyst The process is analternative method for continuous transesterification and can use awide variety of feedstock does not consume the catalyst reducesthe reaction time from hours to seconds and does not use water ordangerous chemicals [164647] Treatment of the lipids extractedfrom Dunaliella tertiolecta and Nannochloropsis oculata with Mcgyanprocess to produce biodiesel reached up to 85 in the conversion oftriacylglycerides and free fatty acids to alkyl esters [48]

Alternatively by shifting the production route microalgal oilscan be used to produce ldquogreen dieselrdquo by a process known ascatalytic hydroprocessing The basic difference of this with trans-esterification is the usage of hydrogen rather than the alcohol Alsothe by-products like propane water and carbon dioxide differfrom glycerol of transesterification [816] Green diesel has super-iority over biodiesel with its lower oxygen constitution similar tothe petroleum derived fuels with a near zero oxygen content Theprimary goal of the processes is to produce a minimized oxygencontaining green diesel with maximized final energy content[816] Also because of the high paraffinic hydrocarbon contentgreen diesel has higher cetane numbers and energy content onmass basis compared to biodiesel Using the microalgal oils forgreen diesel will be advantageous because of the applicationpotential in the conventional petroleum refinery systems with

existing infrastructure and the by-products (H2O and CO2) can berecycled to be used in the microalgae cultivation again

With the rapid progress in the area of genetic engineering theresearchers can now present the genome sequences of microalgaefor example a lipid producing microalgae specie that has potentialin biofuel production ie Nannochloropsis gaditana genome isnewly finalized and may become a model organism like Chlamy-domonas reinhardtii Chlorella variabilis Micromonas pusila Ostreo-coccus tauri Ostreococcus lucimarinus Thalassiosira psudonanaEmiliana huxleyii Fragilariopsis cylindrus Aerococcus aophageffe-rens Cyanidioschyzon merolae and Phaeodactylum tricornutum withcompleted genomes [4950] By understanding these model micro-organisms in molecular basis we can have the chance to improveproductivities in future applications

The ultimate idea was the excretion of the oils from themicroalgae cells without the need of extraction step This ideawas supported with the studies focusing on Escherichia coli andSaccharomyces cerevisiae to excrete lipids through membraneswith genetic engineering tools [5152]

22 Biohydrogen

Hydrogen with its unique properties is accepted to be arenewable sustainable and environmentally friendly energy car-rier that serve as one of the most promising alternative solution toovercome the growing environmental concerns considering thefuture energy demands [5354]

Today there are various conventional as well as novel strategiesto produce hydrogen from fossil fuels (steam reforming plasmareforming thermal cracking gasification) biomass (pyrolysismicrobial conversion syngas conversion supercritical conversiongasification) and water (photolysis thermolysis electrolysis)incorporating chemical and biological processes [272955] Evenif the hydrogen production is dominated by the chemical pro-cesses using fossil fuels biological processes started to get moreattention since the first studies in the 1920s [56ndash58]

The metabolic routes for biohydrogen production differ accord-ing to the microorganism [2759]

Microalgae

(a) Direct photolysis 2H2O-light-2H2+O2

(b) Indirect photolysis(1) 12H2O+6CO2-light-C6H12O6+6O2

(2) C6H12O6+12H2O-12H2+6CO2Photosynthetic bacteria(a) Photofermentation CH3COOH+2H2O-light-4H2+2CO2

(b) Water-gas shift CO+H2O-H2+CO2Anaerobic bacteria Dark fermentationC6H12O6+2H2O-4H2+2CO2+2CH3COOH

Related with their photosynthetic productivity and light utili-zation efficiency microalgae can perform special biochemical andphotochemical reactions with minimum requirements that makehydrogen production possible under aerobic and anaerobic envir-onments [60ndash62]

Microalga like Anabaena sp [6364] Chlorella pyrenoidosa [65]Chlorella vulgaris [66] Platymonas subcordiformis [6667] Spirulinaplatensis [68] and especially Chlamydomonas reinhardtii [6970] getattention in biohydrogen production

Microalgae use two classes of oxygen sensitive metalloenzymesnitrogenases and hydrogenases that are closely related with thefinal biohydrogen generation process in photosynthesis [6371]

There are several types of hydrogenases like the hup-encodedNiFe-uptake hydrogenases hox-encoded NiFe-bidirectional hydro-genases FeFe hydrogenases NiFeSe-bidirectional hydrogenases

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 249

and Fe-only hydrogenases utilized by bacteria and microalgae Onthe other hand nitrogenases of purple non-sulfur bacteria andheterocyst microalgae can be classified by their metal cofactor asmolybdenum iron and vanadium types [7273]

Nitrogenase is the part of the biological nitrogen fixation andhydrogenase is capable to catalyze hydrogen consuming reactionsBiohydrogen production based on these enzymes differs in energyconsumption Hydrogenase mediated reactions are about threetimes more efficient than nitrogenase catalyzed reactions based onspent energy in the form of ATP On the other hand nitrogenasesare relatively less sensitive to oxygen compared to hydrogenases[74ndash76] Relatively or not because both enzymes are sensitive tooxygen it is important to control culture conditions for optimalhydrogen production

Microalgal biohydrogen production can take place duringphotosynthesis from water by the two photosystems dark fer-mentation of the reduced carbon produced by photosynthesis andphotofermentation by the enzymatic oxidation of intracellularreductants derived from fermentation [77ndash80]

Even if the studies on microalgal biohydrogen started in the 1930s[568182] it was shown that the production can be achieved by theinactivation of photosynthetic water oxidizing activity catalyzed bythe reaction center of photosystem two (PSII) [83ndash85] the productiv-ities could not reach to meaningful levels until there was a novelprotocol depending on sulfur deprivation [69] This protocol dependson the succession of photosynthetic reactions in which oxygenproduction and carbon accumulation take place and anaerobic photo-reactions through which the consumption of stored photosyntheticcellular metabolites for biohydrogen generation take place Sulfurdeprivation triggers the conversion of PSII centers to an intermediatein the PSII repair cycle in other words from a QB-reducing to aQB-nonreducing form resulting in the decrease of photosyntheticoxygen evolution capacity [86ndash88]

Compared to the other methods like using inhibitors (DBMIBDCMU SAL C1-CCP etc) or alternating lightdark cycle the removalof sulfate from the growth medium achieves a reversible inactiva-tion with sustainable and increased hydrogen production [83ndash85]

Most of the recent studies focused on the two stage sulfurdeprivation protocol however as summarized by some of theexample studies from batch to continuous processes with variousprocedures the use of different microalgae is a good sign of theprogress towards the future (Table 4) But again some microalgaelike Platymonas subcordiformis Platymonas helgolandica or Chla-mydomonas moewusii are not sensitive to sulfur deprivation aswell as Chlamydomonas reinhardtii so utilization of inhibitors andnitrogen starvation enhance the hydrogen production [8990]

Also the outdoor studies point out another bottleneck in theproductions Even if the applications in lab scale are givingpromising results outdoor cultures still cannot reach the compar-able levels Microalgae cells have problems to tolerate the lightinhibition and sulfur deprivation when exposed to direct sunlightoutdoors They need to be acclimated to light before the hydrogenproduction phase [91]

Besides the studies on the enhancement of the biohydrogenproduction focusing on culture techniques like utilization of immobi-lized microalgae or stressed cultivations with regard to light andmedium components the progress in genetic engineering to improveproduction levels focuses on engineering truncated antennas of thespecies for better sunlight utilization outdoors without inhibition orengineering oxygen tolerant species that can produce hydrogen inaerobic conditions which is still under investigation [7392]

23 Bioethanol

Bioethanol may be considered as an alternative clean burningfuel because of its environmentally friendly combustion products

with low greenhouse gas effect relative to fossil fuels Todaycommercial bioethanol production is mainly from agriculturalstocks and raw materials like corn rice wheat cassava sugarcane sugar beet and sweet sorghum through biochemical orthermochemical processes [161793] Even though the route ofproduction depends on the raw material it can be summarized asthe breaking of the biomaterial to simple sugars that furtherfermented using alcohol producing microorganisms The producedethanol later separated and concentrated through downstreamprocesses (Fig 4)

Facing the conflict of global energy and food demand therehave been increasing interest and worldwide studies in producingbioethanol from alternative sources like microalgae rather thanfeedstock that has minor impact in the daily life [161793]

Bioethanol from microalgae can be produced through thefermentation of the microalgal biomass or directly through cellularreactions [9495]

When considering ethanol production via fermentation the keyis the accumulation of starch which is a potential substrate thatcan reach half of the microalgas cellular dry biomass Microalgalstarch can be extracted by mechanical or enzymatic means andfurther separated by downstream processes incorporating wateror an organic solvent This starch will be hydrolyzed to glucose tobe used in ethanol fermentation [9697] Production mainly differsfrom other crop raw materials in the first steps of the processbecause microalgae will need special concentration harvestingand mechanical disruption systems related with their cellularphysiology and culturing [98]

Microalgae can also excrete ethanol directly through the cellwalls by means of intracellular processes under dark becauseillumination prevents the formation of ethanol except for minoramounts This process which is reported in some microalgae likeChlorococcum littorale [99] Chlamydomonas reinhardtii [8384]Chlamydomonas moewusii [100] Chlorella vulgaris [101] Oscilla-toria limnetica [102] Oscillatoria limosa [99] Gleocapsa alpicola[103] Spirulina platensis [68] Cyanoteche sp [99] covers theanaerobic metabolism in algae where the assimilation and forma-tion of hydrogen carbon dioxide formate acetate ethanol lactateglycerol and butannediol take place [1783] Degradation of intracel-lular starch which is the main endogenous carbon source storedduring aerobic phototrophic metabolism to pyruvate is accomplishedby the EmbdenndashMeyerhofndashParnas and pentose phosphate pathwaysusing pyruvate decarboxylase and alcohol dehydrogenase enzymes[99102] As stated by Gfeller and Gibbs [83] the lack of ethanolproduction by the microalgae cells during illumination is related withthe absence of available reduced pyridine nucleotides with theassumption of active acetaldehyde and alcohol dehydrogenases Twopossible conversion routes for acetyl-CoA to acetate and ethanol canbe followed In the former route half of the acetyl-CoA is converted toacetate by a deacylase while the rest is reduced to ethanol withacetaldehyde as intermediate In the latter route acetyl-CoA is reducedto acetaldehyde that undergoes a dismutation sequence until theformation of acetate and ethanol [8384]

Enhancing direct microalgal bioethanol production by geneticmanipulations is also under consideration Genes from the ethanolproducing bacterium Zymomonas mobilis was transfered intomicroalgae Synechococcus sp aiming to give the ability to utilizethe fixed carbon for direct ethanol excretion to the culture volumethrough the cell walls [93104]

The novelty of the process lies in the separation of producedbioethanol from the culture medium This process eliminates theharvesting step that decreases the energy costs and water usageassociated with the separation processes required for algae har-vesting and fuel extraction [94105]

Besides bioethanol being the main product the remainingmicroalgal biomass may be used to produce biomethane again

Table 4Microalgal hydrogen production

Microalgae Cultivation Process PBR type Culture medium Hydrogen productionprocedure

Time H2 production Refs

Anabaena variabilis (CCAP 14034B)

Continuousndashphotoautotrophic

Lab Stirred (300 mL) Nitrogen free Allen-Arnon

Nitrogen free Allen-Arnon medium

Under vacuum for 15 min Increased light intensity for

5 h at the 6th day ofcultivation

35 days 12ndash14 mL gminus1DW hminus1 [164]

Anabaena variabilis (ATCC 29413) Continuousndashphotoautotrophic

Lab Vial (14 mL) Allen-Arnon(containing Na2MoO4 orNa3VO4 or neither)

Under argon flushing 80ndash100 h

Up to 5 nmol hminus1 mg Chlaminus1 at pH levels of 7ndash9 with Na3VO4 added cultures

[165]

Anabaena sp PCC 7120 (3hydrogenase mutants from PCC7120)

Batchndashphotoautotrophic Lab Sealed polystyrenecuvettes (1 cm light path47 mL capacity)

BG 11 Nitrogen free BG 11 medium Under anaerobic conditions Various light intensities

32ndash40 h Up to 08ndash1 mmol per cuvette (47 mL) [63]

Anabaena sp PCC 7120 and itsmutant AMC 414

Continuousndashphotoautotrophic

Outdoor Tubular-coiled (435 L) BG 11 Nitrogen free BG 11 medium Under argon atmosphere Nitrogen free BG 11 medium Under anaerobic conditions Increased light intensity

7 days 149 mL hminus1Lminus1PBR (373 mL total) with themutant

[166]

Anabaena variabilis (ATCC 29413) Batchndashphotoautotrophic Lab Panel (500 mL capacity) BG 11 50 h Up to 40ndash50 mL [167]

Chlamydomonas reinhardtii(CC124)

BatchndashphotomixotrophicSynchronous andunsynchronous growth

Lab Stirred glass bottles(12L)

TAP TAP-S medium (transferred bycentrifugation)

140 h 102 mL (with 4 h synchronizedcultures)

86 mL (with unsynchronized cultures)

[168]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotomixotrophic Lab Stirred glass bottles(500 mL)

TAP TAP-S medium transfer bycentrifugation

TAP-S medium inoculationby TAP culture (10inoculation)

175 mL Lminus1 (with centrifuged cultures under20ndash40 mE mminus2sminus1 average light intensity)

[87]

Chlamydomonas reinhardtii(CC124)

Continuousndashphotomixotrophic

Lab Stirred glass bottles(1050 mL)

TAP-S (90 mmol sulfateadded)

TAP-S medium two stagechemostat with aerobicstage and anaerobic stage

TAP-S medium TAP medium with limiting

sulfate (10ndash20 mM) Anaerobic conditions Sulfur free medium Anaerobic

4000 h Up to 058 mL hminus1Lminus1PBR [169]

Chlamydomonas reinhardtii (Dang137C mt+ and a nonmotilemutant CC 1036 pf18 mt+)

Batchndashphotomixotrophic-immobilized

Lab Panel (160 mL) TAP (046 mM sulfatereplete)

23 days 45 mL dayminus1 (380 mL total) [170]

Chlamydomonas reinhardtii (Dang137C mt+)

Batch-photoautotrophicmixotrophic andheterotrophic

Lab Flat glass bottles PBR(15 L volume)

HS (CO2 bubbling) TAPwith or without CO2

bubbling

60ndash80 h 11704 mmol Lminus1 (sim28 mL (hL)minus1) inphotoautotrophic cultures

45716 mmol Lminus1 (sim40 mL (hL)minus1) inphotoheterotrophic cultures

09708 mmol Lminus1 (sim69 mL (hL)minus1)inphotomixotrophic cultures

[171]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotoautotrophic Lab Flat glass bottles PBR(15 L)

High salt HS sulfur free medium Argon purging during the

first 24 h of deprivation TAP-S medium Various dilutions Anaerobic conditions

100 h 7173 mL Lminus1 (175 mE mminus2sminus1 lightintensity pH 77)

5272 mL Lminus1 (420 mE mminus2sminus1 lightintensity pH 74)

[172]

Chlamydomonas reinhardtii(CC124)

Semi continuousndashphotomixotrophic

Lab Stirred tank (25 L) TAP 127 days 1108 mL [173]

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic-immobilized

Lab Vials (75 mL) TAP TA-S-P (no sulfate nophosphate) medium

Alginate entrapped

160ndash180 h

0307002 mol mminus2 (125 mmol mgminus1 Chl hminus1) [174]

Batchndashphotomixotrophic Lab Glass bottles (325 mL) TAP 192 h 395 mmol106 cellsminus1 hminus1 with TAP-S [90]

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harvested cells flushed withor without argon

Anaerobic conditions TAP-S or TAP-N DCMU mixed ethanol

addition Dark anaerobic

fermentation

Chlamydomonas reinhardtii(CC124)

34 mmol106 cellsminus1 hminus1 with TAP-N

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Stirred tank (1 255 L) TAP-S TAP-S medium transfer bycentrifugation

Various mixing time Various light energy Scale-up

192 h Max with 122 kJ sminus1 mminus3 light energy and25 min mixing time

[202]

1 L PBR 1537005 mL Lminus1 hminus1

25 L PBR 1327005 mL Lminus1 hminus1

5 L PBR 1027005 mL Lminus1 hminus1

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Tubular (110 L) TAP-S TAP-S medium transfer bycentrifugation

Modified with silicananoparticle to enhancescattering

48 h 3121571789 mL (06 mL Lminus1 hminus1) [203]

Chlorella pyrenoidosa C-101 Batchndashphotoautotrophic Lab Bubble column (650 mL) Modified Bristol Nitrogen flushing under dark forldquo420rdquo h

60ndash65 h 6910minus2 m3 kgminus1 cell [65]

Chlorella vulgaris MSU 01 Batchndashphotomixotrophic Lab Stirred (500 mL) Modified BG11 and MJ Anaerobic conditions Corn stalk as carbon source

in the medium

6ndash7 days 26 mL [175]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Dark incubation Anaerobic nitrogen

atmosphere Addition of specific effectors

(DCMU DCCD DBMIBand CCCP)

Continuous illuminationafterwards

8 h 0339 mL hminus1 Lminus1 (144 mL) based on1106 cells mLminus1 at 15 μM CCCP addedculture after 8 h of illumination

[66]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Sulfur deprive medium Incubation under dark Anaerobic conditions Continuous illumination

afterwards

50 h 11720 nL hminus1 (with seawater-S medium) [67]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Torus (15 L) Defined mineral Dark incubation Anaerobic nitrogen

atmosphere 15 μM CCCP addition Continuous illumination

afterwards

4ndash6 days 720 mL hminus1 (2366770 mL) [176]

Platymonas helgolandica vartsingtaoensis

Batchndashphotoautotrophic Lab Jars (130 mL) F2 Anaerobic Illuminated -S medium Dark CCCPDCMU or both

added medium

25 h 0002 mmol Lminus1 withndashS medium 0160 mmol Lminus1 with CCCP medium 0014 mmol Lminus1 with DCMU medium 0290 mmol Lminus1 with CCCP

+DCMU medium

[89]

Spirulina platensis (NIES-46) Batchndashphotoautotrophic Lab Erlenmeyer flasks(60 mL)

SOT Nitrogen free medium Under dark

20 h 2 mmol mgDWminus1 [68]

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Table

4(con

tinu

ed)

Micro

alga

eCu

ltivation

Pro

cess

PBRtype

Culture

med

ium

Hyd

roge

npro

duction

pro

cedure

Time

H2pro

duction

Refs

Anae

robicco

nditions

Syne

chocystissp

PCC68

03an

dits

mutantNDH-1

complex

defi

cien

tM55

Batch

ndashphotoa

utotrop

hicndash

encapsu

lated

Lab

Vials

(2mL)

BG

11

Nitroge

natmosphere

Under

cycled

lightan

ddark

exposure

5day

s0005

ndash004

5mM

[177

]

Tetraspo

rasp

CU25

51Batch

ndashphotom

ixotrophic

Lab

Vials

TAP(w

itho

rwithou

t05mM

β-mercaptoethan

olfor

24h)

Su

lfuran

dnitroge

ndep

rive

dmed

ium

Argon

flush

edan

aerobic

atmosphere

424

h173ndash61

7mm

olmgminus

1Chlahminus1

[178

]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264252

through anaerobic digestion for electricity generation The carbondioxide and discharged water formed as by-products of thefermentation can be recycled for the microalgae cultivation tofulfill the biorefinery concept [94105]

24 Biomethane

Today agricultural plants or by-products are conventionalsources for renewable biogas production which is mainly amixture of methane (55ndash75) and carbon dioxide (25ndash45) byanaerobic digestion Biomethane from the biogas can be used as afuel for transportation and electricity generation or for heatingpurposes especially in the rural areas [16106107]

Microalgae with their dominancy over crop plants by means ofproductivity per hectare triggered the attention for the production ofbiogas The solar energy converted and stored by the microalgae cellsthrough photosynthesis can be transformed into energy through theanaerobic digestion to produce methane [106108]

Microalgal biomass having high cellular lipid starch andprotein low cellulose and on the other hand the absence of ligningives a reliable and effective anaerobic digestion These specifica-tions make microalgae a good alternative for effective biomethaneproduction compared to the other crop plants [16107108]

Microalgal biomass can be processed anaerobically step by stepwith specialized groups of bacteria [109]

Hydrolyzation of biopolymers to monosaccharides by hydro-lytic bacteria

Fermentation of the monosaccharides to carboxylic acids andalcohols by fermentative bacteria

Conversion of the acids and alcohols to acetate hydrogen andcarbon dioxide by acetogenic bacteria

Conversion of the end products of acetogenic reactions tomethane and carbon dioxide by methanogenic bacteria

Microalgal biomass remaining after the anaerobic digestion canbe further processed to make fertilizers that can add an extra valueto the overall process Also the carbon dioxide portion of theproduced biogas can be recycled again to cultivate the neededmicroalgal biomass for processing [107110ndash112]

A predicted model of microalgae biomass for digestion toproduce electrical and thermal energy discussed the economicprofitability related with technical aspects of the productionsystem The results showed that the microalgae productivityharvesting concentration and usage of high rate anaerobic diges-ters are the key factors for the economic energy production [113]

A life cycle perspective study using a stochastic model indi-cated that when compared with the conventional crops likeswitch grass canola and corn the environmental impact ofmicroalgal biomass production is higher with respect to energydemand greenhouse gas emissions and water use regardless ofcultivation location Only in overall land use and eutrophicationpotential microalgae present favorable results [114] This mayseem to be a disadvantage to produce biomethane from microalgalbiomass but the studies also supported that the integratedprocesses using proper photobioreactors combining microalgaecultivation and waste water treatment systems for biomethaneproduction will help to reduce the environmental impacts result-ing in a competitive and effective production [11416115]

25 Integrated processes

Relations between parameters and the target products (bio-mass lipid hydrogen ethanol) are important in the selection ofthe microalgae for efficient biofuel production As can be followedfrom the tables summarizing the microalgal biofuel productions

Sugars

- Sugarcane juice

- Molasses

- Sugar beet

Starch

- Corn

- Oats

- Wheat

- Sago Palm

- Cassava

- Banana wastes

- Rye

- Barley

- Triticale

- Sorghum

- Algal biomass

Lignocellulosic materials

- Crop residues

- Cellulose wastes

- Hardwood

- Harbaceous biomass

- Softwood

- Municipal solid wastes

Fermentation

- Saccharomyces cerevisiae

- Schizosaccharomyces pombe

- Zymomonas mobilis

- Saccharomyces bayanus

- Pichia stipitis

- Candida shehatae

- Pachysolen tannophilus

- Mucor indicus

- Chalara parvispora

- T thermosaccharolyticum

- T Ethanolicus

- B Stearothermophilus

- C thermohydrosulfuricum

- C thermocellum

- Milling

- Grinding

- ShredingBreaking hemicellulose

chains

- Physical

- Chemical

- Physicochemical

- Biological

Hydrolization -Detoxification

-Neutralization

Sugars

- Hexoses

- Pentoses

Separation and

Concentration

- Distillation

- Rectification

- Dehydration

ETHANOL

Fig 4 Ethanol production from biomass productionSource Adapted from Refs [9398201]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 253

studies focus on the separation of production processes into twomain steps growth mediated and product mediated When con-sidering direct biofuel production the main approach is product

mediated for higher lipid hydrogen or ethanol production Whenconsidering biofuel production integrated with other microorgan-isms (Table 5) the main approach is growth mediated for higher

Table 5Integrated biofuel processes working with microalgae

Microalgae System Product Ref

Chlamydomonas reinhardtii (UTEX 90) Enzymatic treatment of algal biomass and conversion to ethanol by Saccharomyces cerevisiae Ethanol [179]Chlamydomonas reinhardtii (UTEX 90) Hydrothermal acid treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [180]Chlorella vulgaris (IAM C-534) Enzymatic treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [181]Synechococcus leopoliensis (IAMM 6) Fermentation of acid treated saccharified algal biomass by yeast Saccharomyces sake (IFO 2347) Ethanol [97]Chlamydomonas reinhardtii Chlorella vulgaris (macroalgae Undaria pinnatifida) Enzymatic treatment of pre-acid hydrolyzed algal biomass fermentation by 4 different strains of Escherichia coli Ethanol [182]Schizocytrium sp Fermentation of hydrothermal treated algal biomass by E coli KO11 Ethanol [183]Microcystis aeruginosa and Anabaena variabilis Hydrolysis and fermentation of Super Critical fluid pretreated algal biomass by Saccharomyces cerevisiae Ethanol [204]Scenedesmus obliquus Fermentation of algal biomass hydrolysate by Kluyveromyces marxianus IGC 2671 Saccharomyces carlsbergensis

ATCC6269 and Saccharomyces bayanusEthanol [205]

Anabaena sp PCC7120 Fermentation of hydrogen produced residual algal biomass by Enterobacter aerogenes Hydrogen [184]Arthrospira (Spirulina) platensis Nannochloropsis sp and Dunaliella tertilecta Anaerobic fermentation of thermal pretreated algal biomass by immobilized Clostridium acetobutylicum Hydrogen acetone

ethanol butanol[206]

Chlorella vulgaris ESP6 Dark fermentation of acid or alkalineenzyme pretreated algal biomass hydrolysate by Clostridium butyricumCGS5

Hydrogen [207]

Chlorella sp Simultaneous hydrolysis and fermentation of algal biomass by sewage sludge consortia Hydrogen [208]Thalassiosira weissflogii Dark fermentation of algal biomass with the thermophilic bacterium Thermotoga neapolitana Hydrogen [209]Chlamydomonas reinhardtii (IAM C-238) Chlorella pyrenoidosa (IAM C-212) andDunaliella tertiolecta (ATCC 30909)

Fermentation of algal biomass by Lactobacillus amylovorous (ATCC 33620) and Rhodobacter sphaeroides RV Hydrogen [185]

Chlamydomonas reinhardtii (IAM C-238) and Dunaliella tertiolecta (ATCC 30909) Fermentation of algal biomass by Lactobacillus amylovorous and Rhodobium marinum (A-501) mixed culture Hydrogen [186]Chlamydomonas (MGA 161) Fermentation of algal biomass by Rhodovulum sulfidophilum (W-1S) Hydrogen [85]Chlamydomonas reinhardtii (C238) Mixed cultivation of Chlamydomonas reinhardtii (C238) with Rhodospirillum rubrum (NCIB 8255) Hydrogen [187]Scnedesmus sp Fermentation of algal biomass by anaerobic digested sludge Hydrogen [188]Arthrospira maxima Anaerobic digestion of algal biomass by sewage sludge consortia Methane [210]Phaeodactylum tricornutum Anaerobic digestion of algal biomass by potato factory origin anaerobic granular sludge Methane [211]Scenedesmus sp Anaerobic digestion of high pressure thermal pretreated raw and residue (from lipid extraction) algal biomass

and by anaerobic digestor sludgeMethane [212]

Scenedesmus sp Anaerobic digestion of ultrasound and thermal pretreated raw algal biomass by sugar factory origin anaerobicgranular sludge

Methane [213]

Scenedesmus sp Anaerobic digestion of mild thermal pretreated raw algal biomass by sugar factory origin anaerobic granularsludge

Methane [214]

Spirulina platensis Anabaena variabilis and Chlorella sp Processing of algal biomass by an integrated system of methanogenic culture and Rhodobacter capsulatus Methane and hydrogen [189]Spirulina platensis (UTEX 1926) Rhodotorula glutinis (2541) Mixed cultivation of microalgae and yeast using waste water Lipid (biodiesel) [190]Spirulina platensis Using excess CO2 from the ethanol fermentation by Saccharomyces cerevisiae Lipid (biodiesel) [119]Botryococcus braunii (two strains BB763 and BB764) Chlorella vulgaris Chlorellapyrenoidosa

Biodiesel production catalyzed by immobilized Penicillium expansum lipase and Candida antarctica lipase B(Novozym 435)

Lipid (biodiesel) [191]

Chlorella vulgaris (21111B) Anaerobic digestion of algal biomass by sewage sludge origin methanogenic culture Methane [112]Chlorella sp and Scenedesmus Anaerobic digestion of algal biomass by sewage sludge culture Methane [106]Chlorella sp Anaerobic digestion of algal biomass by sludge culture Methane [192]Arthrospira platensis Chlamydomonas reinhardtii Chlorella kessleri Dunaliellasalina Euglena gracilis and Scenedesmus obliquus

Anaerobic digestion of algal biomass by sewage sludge culture Methane [107]

Spirulina maxima Anaerobic digestion of algal biomass by sewage sludge culture Methane [193]Chlorella sp and Scenedesmus Anaerobic codigestion of algal biomass with waste paper by methanogenic culture Methane [194]Tetraselmis Anaerobic digestion of algal biomass by methanogenic culture Methane [195]Chlorococcum sp Anaerobic treatment of distillery waste with algal biomass by acidogenicmethanogenic culture Methane [196]Phaeodactylum tricornutum (CCAP10551) Anaerobic digestion of algal biomass by granular seed sludge from digester treating potato processing waste

water dominated by Methanosaeta sp and Methanosarcina spMethane [197]

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 255

biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264256

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

SSOncel

Renew

ableand

SustainableEnergy

Review

s26

(2013)241

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 259

technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

[1] EIA (US Energy Information Administration) International Energy Outlook2010 Washington DC 20585 US 2010 langwwweiagovoiafieoindexhtmlrang

[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264262

[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 3: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

Table 2List of companies working on microalgal biofuel technologiesSource Adapted from Refs [139ndash142]

A2Be Carbon Capture Algae Venture Systems Algaewheel AlgaEnergy

AlgoDyne Ethanol Energy Corp Aquaflow Bionomic Aquatic Energy Aurora Algae IncAlgasol Algenol Amyris Biotech Algaecake Tech CorpAXI Algafuel Algae Biotech SA Algae Link NVAirbus Air New Zealand Boeing BioAlgaene LLCBlue Marble Energy Bodega Algae BBI BionavitasBTR Labs Biofuel Systems Biomara Bisantech Nuova GmbHContinental Airlines Cequesta Algae Carbon Capture Corporation CellanamdashShell amp HR BiopetroleumChevron Culturing Solutions Inc Clean Algae SA Circle Biodiesel amp Ethanol CorporationCommunity Fuels Canadian Pacific Algae Center of Excellence for Hazardous

Materials ManagementDynamic Biogenics

Diversified Energy DFI Group ENEL EADS and IGV GmbHEnhanced Biofuels amp Technologies Fluid Imaging Technologies General Atomics Green Gold Algae and Seaweed Sciences IncGeneral Electric GreenFuel Technologies Corporation Greenshift Green Star Products IncGreenbelt Resources Corporation Global Green Solutions Hawaiian Electric Company HR BiopetroleumInventure Chemical Technology Ingrepo Infinifuel Biodiesel International EnergyImperium Renewables Jet Blue Japan Air KelcoKuehnleAgrosystems Kai Bioenergy KLM Airlines LiveFuelsLS9 Synthetic Bioenergy solutions MBD Biodiesel Neptune Neste OilNorthington Energy Organic Fuels OriginOil Ocean Technology amp Environmental ConsultingOilfox Argentina Petro Algae Phycal Pure Power EnergyPetroSun Biofuels Phyco2 Planktonix Corporation ProvironRenewable Energy Group Revolution Biofuels SeaAg SBAE IndustriesSunx Algae Oil Research Lab Solena Group Sapphire Energy SeambioticSolazyme SunEco Sunrise Ridge Solix BiofuelsSolray Synthetic genomics and Exxon Mobil Corp SGC Energia SGPS SA SAIC CorpTexas Clean Fuels Virgin Airways Valcent VG energyW2 Energy XL RenewablesmdashSigmae

Fig 1 Annual publication count and the top 10 countries considering the number of publications and companiesSource Adapted from Refs [139ndash142198]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 243

long-chain saturated and poly-unsaturated fatty acid oils [10ndash12]Fatty acid profiles of the microalgae depend on the species andculture conditions During optimum culture conditions microalgaesynthesize fatty acids (up to 20 of dry cell weight) mainly for

esterification into glycerol based membrane lipids But when facedwith stress conditions microalgae can diverge from lipid produc-tion pathway towards the synthesis and accumulation of neutrallipids that may reach up to 50 dry cell weight mainly in the form

MIC

RO

ALG

AE

Oil Extraction

Hydrotreatment Green Diesel

Transesterification Biodiesel

Fermentation

Ethanol

Hydrogen

Gasification Syngas

Fermentation

Ethanol

Butanol

Butyric Acid

Acetic Acid

Methane

Methanetion Methane

Hydrogen

Anaerobic Digestion Methane

Biophotolysis Hydrogen

Pyrolysis

Bio-oil

Syngas

Charcoal

Fig 2 Biofuel routes from the standpoint of microalgaeSource Adapted from Refs [816108199]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264244

of triacylglycerols which are actually the key component of algallipids for biodiesel production Triacylglycerols are distinct frommembrane glycerolipids because of their character as the storagematerial for energy instead of structural usage [913]

Lipid productivity of a microalga is accepted to be an indicatorof its potential for biodiesel production

Studies focus on different parameters such as nutrient sourcenutrient concentration light intensity salinity pH mixing speed andtemperature to enhance the lipid productivity of the microalgae(Table 3) Microalgae show variable responses to the effects resultingin various lipid productivities For example on cultivation with 10CO2 biomass productivity of the Scenedesmus sp was higher thanBotryococcus branuii on the other hand lipid productivity was lowerbut similar productivities could be seen in the case of flue gas(55 CO2) cultivation [14] In another study results indicated thatpotassium phosphate and magnesium sulfate are the major mediacomponents affecting the lipid productivity of Botryococcus branuiiand the lipid and biomass optimized media should differ in concen-trations [15] The key is to select the proper method of approachconsidering the microalga for the lipid productivity

Extraction of microalgal lipids is the bottleneck for high yield inproductions After the harvest the culture starts its downstreamjourney As a first step the excess water that is an unwantedvolumetric load is removed through concentration processes likefiltration drying flocculation and centrifugation The concentratedcells can either be extracted directly or through a disruption stepin which the intercellular content was released to enhance theextraction process Considering microalgae because the targetproduct oil is trapped inside strong cell walls the disruption stepcan be termed as a part of the extraction step [16ndash18] Microalgaloils could be extracted using milling expeller press high pressurehomogenization solvent enzyme supercritical fluid osmoticshock pulsed electric field microwave or ultrasound techniquesThe selection of the method depends on the specie cost andefficiency as well as the environmental concerns The extractedlipids then passed to the fractionation step where the undesiredpolar lipids and non-acylglycerol neutral lipids (such as free fattyacids hydrocarbons sterols ketones carotenes and chlorophylls)were removed Later the purified product is converted intobiodiesel through the transesterification process [19ndash24]

Table 3Various studies focusing on lipid productivities as the key element for biodiesel production

Microalgae Effect Time Cultivation PBR type Lightintensity(lE mminus2 sminus1)

Temp(1C)

Medium Maximum production Ref

Botryococcus braunii(UTEX 572)

CO2 14 days Batchndashautotrophic Bubble column 150 2571 Modified Chu 13 5517153 mg Lminus1 dminus1 (21 biomass) with10 CO2 enriched air

2065 mg Lminus1 dminus1 (24) with 55 CO2

containing flue gas

[14]

Botryococcus braunii(765)

CO2 28 days Batchndashautotrophic Airlift (3 L) 150710 25 Modified BG11 1174 mg Lminus1dminus1 (12717083 biomass) with20 CO2 enriched air

[143]

Botryococcus braunii(UTEX 572)

Media components 18 days Batchndashautotrophic Bubble column(06 L)

50 22 Modified BG11 019 g Lminus1 dminus1 (6496 biomass) in lipidoptimized media

018 g Lminus1 dminus1 (5956 biomass) in growthoptimized media

[15]

Botryococcus braunii(KMITL 2)

Light intensity light cycle nitrogenphosphorus iron cultivation time salinity

40 days Batchndashautotrophic Flasks (1 L) 0ndash538(LD cycle)

25 Chlorella 54697313 with 200 mE mminus2 sminus1 continuouslight 222 mg Lminus1 phosphorus and a salinity of0 psu

[144]

Chlamydomonasreinhardtii

pH and CO2 31 days Batchndashautotrophic BIOCOIL (15 L) 220 2571 Artificial or wastewater

05057002 g Lminus1 dminus1 (2525 biomass) with 33CO2 at pH 75

[145]

Chlorella vulgaris(CCAP 211)

Temperature nitrogen concentration andextraction techniques

14 day Batchndashautotrophic Erlenmayer flask(2 L)

70 15ndash25 Guillard F2 20227060 mg Lminus1 dminus1 (14717030) at25 1C

20307040 mg Lminus1 dminus1 (15317051) with0375 g Lminus1 nitrogen concentration

[146]

Chlorella sorokiniana(GXNN01)

Carbon sources and concentrations 70 h Batchndashautotrophicheterotrophic

Erlenmayer flask(015 L)

0ndash80 3072 BBM 028870008 g Lminus1 (028770018 g gDWminus1)with acetate

Glucose concentration of 20 mmol Lminus1 gavethe maximal lipid yield

0048 lipid gminus1DW dayminus1 (232) inmixotrophic perfusion (rate 28 L hminus1)culture

[147]

Chlorella minutisima(UTEX LB-2341)

Long term outdoor production 80 days Batch or perfusionautotrophicndashmixotrophic

Cylindrical vessel(20 L10 200 Ltotal)

0ndash700 30ndash35 Enriched sea water [148]

Chlorellaprotothecoides(UTEX 249)

Carbon source concentration nitrogenconcentration salinity pH level andagitation speed

103 h Batchndashautotrophicmixotrophicheterotrophic

Erlenmeyer flasks(01 L)

8W 26 Modified basal 025 g Lminus1 dminus1 (25257007) with 15 g Lminus1

glucose 69 pH 019 g Lminus1 dminus1 (20337513) with 204 gLminus1

glycerol 71 pH 0177001 g Lminus1 dminus1 (23087318) with

205 g Lminus1 acetate 67 pH

[149]

Chlorellaprotothecoides(SAG 3380)

CO2 14ndash15days

Batchndashautotrophicmixotrophic

Erlenmeyer flasks(025 L)

100710 2471 BG11 with Peptone 213725 DW (Mixotrophic 1 glycerol) 115731 DW (Autotrophic) 358715 DW (Mixotrophic N-deprived)

[150]

Chlorella pyrenoidosa Waste water 10 days BatchndashMixotrophic Flasks (01 L) 63 25ndash27 Diluted piggery wastewater

(with 1000 mg Lminus1 COD) [151]

Chlorella pyrenoidosaFACHB-9

Waste water 120 h Batchfedbatchndashmixotrophic

Flasks (05 L) 405 (1410LD cycle)

2771 Soybean process wastewater

04 g Lminus1 dminus1 (377934 DW) with fed batchculture

[152]

AuxenochlorellaprotothecoidesUMN280

CO2 waste water 12 days Batchndashmixotrophic Roux bottles(058 L)

60 2572 Waste water (05 L)and BG11 seed culture(008 L)

0182 g Lminus1 (1866 DW) without CO2

0418 g Lminus1 (2082 DW) with 1 CO2

0516 gLminus1 (2058 DW) with 5 CO2

[153]

Chlorella vulgaris KNO3 CO2 and light intensity 250 h Batch 24ndash120 25 Artificial sea water [154]

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ndash264245

Table 3 (continued )

Microalgae Effect Time Cultivation PBR type Lightintensity(lE mminus2 sminus1)

Temp(1C)

Medium Maximum production Ref

Membrane spargedcylindrical vessel(5 L)

40 mg Lminus1 dminus1 (20) at 60 mE mminus2sminus1 lightintensity 1 mM KNO3 concentration 1 CO2

enrichmentChlorellavulgarisKCT-CAG10032

CO2 14 days Batchndashautotrophic Bubble column 150 2571 BG11 6917003 mg Lminus1dminus1 (7 biomass) with 10 CO2

enriched air[14]

Chlorella vulgarisBEIJ-H14

Glucose and urea 665 h Fed batchndashheterotrophic

Stirred tank (600 L) Dark 36ndash37 Glucose enrichedmedium

97 dry weight [155]

Chlorella vulgarisCCALA 256

Nutrient limitation 8 days Batchndashautotrophic Thin layer (150 L) 100ndash960 195ndash33

14 SS 032670010 g Lminus1 dminus1 (306705 DW) [156]

Choricystis minor Temperature dilution rate andpostharvest methods

Continuousndashautotrophic

Stirred tank (4 L) 550 10ndash30 BG 11 82 mg Lminus1 dminus1 (213717) at 25 1C and adilution rate of 0014 hminus1

Lipid content increased up to 595716under postharvest conditions withoutphosphate and nitrate

[157]

Nannochloropsisoculata

Temperature nitrogen concentration andextraction techniques

14 days Batchndashautotrophic Erlenmayer Flask(2 L)

70 25ndash38 BBM 9117030 mg Lminus1 dminus1 (14927082) at15 1C

16417011 mg Lminus1 dminus1 (15867059) with0075 gLminus1 nitrogen concentration

[139]

Nannochloropsisoculata

Temperature nitrogen and yeast extractconcentrations

16 days Batchndashphotomixotrophic

Airlift (2 L) 160ndash270 15ndash35 F2 10ndash15 (50 ppm nitrogen) 20-25 (125 ppm nitrogen) 25ndash30 (15 1C) 20ndash25 (35 1C)

[158]

Haematococcuspluvialis

Continuous light intensity or light cyclesno nitrogen or no aeration on production

14 days Batchndashautotrophic Flask 90 24 BBM 15617146 DW Under normal conditions 34857078 DW Under full medium

continuous light with aeration 32997277 DW Under continuous light

aeration no nitrogen

[159]

Neochlorisoleoabundans(UTEX-1185)

Nitrogen sources and concentrations 7 days Batchndashautotrophic Bubble column(1 L)

360 3072 SE 0133 g Lminus1 dminus1 (38) with 5 mM sodium nitrateas nitrogen source

[160]

Neochlorisoleoabundans(UTEX-1185)

Temperature CO2 and nitrate 18 days Batchndashautotrophic Bubble column(1 L)

150 26ndash30 BM 56 biomass with nitrogen starvation at 30 1Ctemperature without CO2 in air

[161]

Neochlorisoleoabundans(UTEX-1185)

Nitrogen starvation 140 h Continuousndashautotrophic

Flat panel airlift(1 L)

270 25 BBM 126 g mminus3 dminus1 (23) continuous culture withno mineral limitation with nitrate starvation

20657013 mg Lminus1dminus1 (9 biomass) with10 CO2 enriched air

3944 mg Lminus1 dminus1 (18) with 55 CO2

containing flue gas 16ndash18 DW with nitrogen deplete two stage

process 10ndash12 DW with single stage process

[162]

Scenedesmus spKCTC AG20831

CO2 14 days Batchndashautotrophic Bubble column 150 2571 BG11 [14]

Tetraselmis suecica Light and nitrogen concentration 9 days Batchndashautotrophic Stirred tank (20 L) 363ndash1331 2071 Modified F2 [163]

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 247

The preferred route for biodiesel production from oils istransesterification rather than pyrolysis and micro-emulsionbecause of the cost and quality concerns [25] Transesterificationis simply the reaction between triacylglycerols and an acyl-acceptor which can be carboxylic acids (acidolysis) alcohols(alcoholysis) or another ester (interesterification) [2526] Biodie-sel production from microalgal oils through transesterificationprocess has several steps (Fig 3)

The reaction can be chemically (acid or base) or biologically(enzyme) catalytic or non-catalytic (high pressure process) [27ndash29]

Homogeneous (NaOH CH3ONa KOH KOCH3) and heterogeneous(alkaline earth metal oxides zeolite KNO3 loaded on Al2O3 KNO3Al2O3 BaO SrO CaO MgO) base catalysts are conventionally used forbiodiesel production They are more effective with an oil having free

Strain selection

- Determination of cell culture condition

- Optimization of lipid production conditions

- Scale -up

Photobioreactor

LightCO2 Nutrients

Separation amp

Refining

Acid Water

CatalystAlcohol Glycerol

Temperature

Fig 3 Microalgal biodiesel productionSource Adapted from Refs [7 4647199200]

fatty acid concentration up to 2 resulting in high reaction rates(4000 faster) and conversion efficiency under lower operationtemperatures compared to acid catalysts But considering watercontent and acidity of the biodiesel feedstock acid catalysts arepreferred to prevent saponification Even if acid catalysts are effectivewith non-edible oils their limitations like the need for higher amountsof alcohol higher temperatures and pressures slower reaction ratesresult in lower yields Both homogeneous and heterogeneous acidcatalysts (sulfuric acid hydrochloric acid phosphoric acid and sulfo-nated organic acids) are used especially in two step biodiesel produc-tion where in the first step the oil reacts with alcohol by acid catalystsand later reacted with the base catalyst This procedure is preferredwith high free fatty acid concentrated oils where the proceduredecreases the value of the free fatty acids to operational levels [1030]

Water

Biomass Harvesting

- Filtration

- Centrifugation

- Sedimentation

- Flotation

Dryer

Oil Extraction

-Chemical

-Biochemical

-Mechanical

Catalyst

-Chemical

-Biological

Oil

Alcohol

Transesterification

Biodiesel

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264248

Conventional technology of chemical catalysis has some con-straints due to the environmental problems related with soapformation and energy demand due to the downstream processesto recover glycerol and catalysts [262831]

Biological catalysis has some advantages over the chemicalcatalysis including lower energy demand moderate reaction con-ditions lower alcohol to oil ratio easier product recovery and highconversion [3132]

Lipases are the key biocatalysts that are used in biodieselproduction Major producer microorganisms for lipases are Aspergil-lus niger Aspergillus oryzae Bacillus pumilis Burkholderla cepaciaCandida antarctica Candida cylindracea Candida lipolytica Candidaparalipolytica Candida rugosa Chromobacterium viscosum Enterobac-ter aerogenes Eremothecium ashbyii Escherichia coli Geotrichumcandidum Mucor miehei Penicillium cyclopium Penicillium expansumPenicillium restrictum Pseudomonas cepacia Pseudomonas fluorescensPseudomonas fragi Rhizopus arrhizus Rhizopus delemar Rhyzomucormiehei Rhizopus oryzae Saccharomyces cerevisiae and Thermomyceslanuginosus which are also commercially important to meet theneeds of the large scale biodiesel processes [3334]

Main bottlenecks of this process include high cost of enzymelow yield due to inactivation longer reaction time slower reactionrate and the amount of water and organic solvents in the reactionmixture [2532]

The limitations in the biocatalysis are managed via the immo-bilization of the lipases in packed bed reactors to prevent washoutand inactivation [35] using whole cell immobilization [26] ionicliquids in enzyme catalysis [3136] genetic modifications andrecombinant microorganisms to enhance the efficiency and theproduction of the enzyme [26] alternative acyl acceptors [37]stepwise processes [3839] moderate polar solvents [40] non-catalytic methods under supercritical conditions [4142] and highpressure processes to stabilize the enzymes [4344]

From the economical point of view which is also importantchemical catalysis is reported to be cheaper than biologicalcatalysis But the modifications like using immobilized biocatalystsand the enhanced reuse can serve a competitive cost compared tothe chemical catalysts [45]

Numerous approaches are still in progress for the optimizationof the biodiesel production process adaptable to different feedtypes compositions and downstream requirements One of thenovel processes mentioned in recent studies is the ldquoMcgyan Processrdquothat consists of a continuous fixed bed reactor that can producebiodiesel using a metal oxide based catalyst The process is analternative method for continuous transesterification and can use awide variety of feedstock does not consume the catalyst reducesthe reaction time from hours to seconds and does not use water ordangerous chemicals [164647] Treatment of the lipids extractedfrom Dunaliella tertiolecta and Nannochloropsis oculata with Mcgyanprocess to produce biodiesel reached up to 85 in the conversion oftriacylglycerides and free fatty acids to alkyl esters [48]

Alternatively by shifting the production route microalgal oilscan be used to produce ldquogreen dieselrdquo by a process known ascatalytic hydroprocessing The basic difference of this with trans-esterification is the usage of hydrogen rather than the alcohol Alsothe by-products like propane water and carbon dioxide differfrom glycerol of transesterification [816] Green diesel has super-iority over biodiesel with its lower oxygen constitution similar tothe petroleum derived fuels with a near zero oxygen content Theprimary goal of the processes is to produce a minimized oxygencontaining green diesel with maximized final energy content[816] Also because of the high paraffinic hydrocarbon contentgreen diesel has higher cetane numbers and energy content onmass basis compared to biodiesel Using the microalgal oils forgreen diesel will be advantageous because of the applicationpotential in the conventional petroleum refinery systems with

existing infrastructure and the by-products (H2O and CO2) can berecycled to be used in the microalgae cultivation again

With the rapid progress in the area of genetic engineering theresearchers can now present the genome sequences of microalgaefor example a lipid producing microalgae specie that has potentialin biofuel production ie Nannochloropsis gaditana genome isnewly finalized and may become a model organism like Chlamy-domonas reinhardtii Chlorella variabilis Micromonas pusila Ostreo-coccus tauri Ostreococcus lucimarinus Thalassiosira psudonanaEmiliana huxleyii Fragilariopsis cylindrus Aerococcus aophageffe-rens Cyanidioschyzon merolae and Phaeodactylum tricornutum withcompleted genomes [4950] By understanding these model micro-organisms in molecular basis we can have the chance to improveproductivities in future applications

The ultimate idea was the excretion of the oils from themicroalgae cells without the need of extraction step This ideawas supported with the studies focusing on Escherichia coli andSaccharomyces cerevisiae to excrete lipids through membraneswith genetic engineering tools [5152]

22 Biohydrogen

Hydrogen with its unique properties is accepted to be arenewable sustainable and environmentally friendly energy car-rier that serve as one of the most promising alternative solution toovercome the growing environmental concerns considering thefuture energy demands [5354]

Today there are various conventional as well as novel strategiesto produce hydrogen from fossil fuels (steam reforming plasmareforming thermal cracking gasification) biomass (pyrolysismicrobial conversion syngas conversion supercritical conversiongasification) and water (photolysis thermolysis electrolysis)incorporating chemical and biological processes [272955] Evenif the hydrogen production is dominated by the chemical pro-cesses using fossil fuels biological processes started to get moreattention since the first studies in the 1920s [56ndash58]

The metabolic routes for biohydrogen production differ accord-ing to the microorganism [2759]

Microalgae

(a) Direct photolysis 2H2O-light-2H2+O2

(b) Indirect photolysis(1) 12H2O+6CO2-light-C6H12O6+6O2

(2) C6H12O6+12H2O-12H2+6CO2Photosynthetic bacteria(a) Photofermentation CH3COOH+2H2O-light-4H2+2CO2

(b) Water-gas shift CO+H2O-H2+CO2Anaerobic bacteria Dark fermentationC6H12O6+2H2O-4H2+2CO2+2CH3COOH

Related with their photosynthetic productivity and light utili-zation efficiency microalgae can perform special biochemical andphotochemical reactions with minimum requirements that makehydrogen production possible under aerobic and anaerobic envir-onments [60ndash62]

Microalga like Anabaena sp [6364] Chlorella pyrenoidosa [65]Chlorella vulgaris [66] Platymonas subcordiformis [6667] Spirulinaplatensis [68] and especially Chlamydomonas reinhardtii [6970] getattention in biohydrogen production

Microalgae use two classes of oxygen sensitive metalloenzymesnitrogenases and hydrogenases that are closely related with thefinal biohydrogen generation process in photosynthesis [6371]

There are several types of hydrogenases like the hup-encodedNiFe-uptake hydrogenases hox-encoded NiFe-bidirectional hydro-genases FeFe hydrogenases NiFeSe-bidirectional hydrogenases

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 249

and Fe-only hydrogenases utilized by bacteria and microalgae Onthe other hand nitrogenases of purple non-sulfur bacteria andheterocyst microalgae can be classified by their metal cofactor asmolybdenum iron and vanadium types [7273]

Nitrogenase is the part of the biological nitrogen fixation andhydrogenase is capable to catalyze hydrogen consuming reactionsBiohydrogen production based on these enzymes differs in energyconsumption Hydrogenase mediated reactions are about threetimes more efficient than nitrogenase catalyzed reactions based onspent energy in the form of ATP On the other hand nitrogenasesare relatively less sensitive to oxygen compared to hydrogenases[74ndash76] Relatively or not because both enzymes are sensitive tooxygen it is important to control culture conditions for optimalhydrogen production

Microalgal biohydrogen production can take place duringphotosynthesis from water by the two photosystems dark fer-mentation of the reduced carbon produced by photosynthesis andphotofermentation by the enzymatic oxidation of intracellularreductants derived from fermentation [77ndash80]

Even if the studies on microalgal biohydrogen started in the 1930s[568182] it was shown that the production can be achieved by theinactivation of photosynthetic water oxidizing activity catalyzed bythe reaction center of photosystem two (PSII) [83ndash85] the productiv-ities could not reach to meaningful levels until there was a novelprotocol depending on sulfur deprivation [69] This protocol dependson the succession of photosynthetic reactions in which oxygenproduction and carbon accumulation take place and anaerobic photo-reactions through which the consumption of stored photosyntheticcellular metabolites for biohydrogen generation take place Sulfurdeprivation triggers the conversion of PSII centers to an intermediatein the PSII repair cycle in other words from a QB-reducing to aQB-nonreducing form resulting in the decrease of photosyntheticoxygen evolution capacity [86ndash88]

Compared to the other methods like using inhibitors (DBMIBDCMU SAL C1-CCP etc) or alternating lightdark cycle the removalof sulfate from the growth medium achieves a reversible inactiva-tion with sustainable and increased hydrogen production [83ndash85]

Most of the recent studies focused on the two stage sulfurdeprivation protocol however as summarized by some of theexample studies from batch to continuous processes with variousprocedures the use of different microalgae is a good sign of theprogress towards the future (Table 4) But again some microalgaelike Platymonas subcordiformis Platymonas helgolandica or Chla-mydomonas moewusii are not sensitive to sulfur deprivation aswell as Chlamydomonas reinhardtii so utilization of inhibitors andnitrogen starvation enhance the hydrogen production [8990]

Also the outdoor studies point out another bottleneck in theproductions Even if the applications in lab scale are givingpromising results outdoor cultures still cannot reach the compar-able levels Microalgae cells have problems to tolerate the lightinhibition and sulfur deprivation when exposed to direct sunlightoutdoors They need to be acclimated to light before the hydrogenproduction phase [91]

Besides the studies on the enhancement of the biohydrogenproduction focusing on culture techniques like utilization of immobi-lized microalgae or stressed cultivations with regard to light andmedium components the progress in genetic engineering to improveproduction levels focuses on engineering truncated antennas of thespecies for better sunlight utilization outdoors without inhibition orengineering oxygen tolerant species that can produce hydrogen inaerobic conditions which is still under investigation [7392]

23 Bioethanol

Bioethanol may be considered as an alternative clean burningfuel because of its environmentally friendly combustion products

with low greenhouse gas effect relative to fossil fuels Todaycommercial bioethanol production is mainly from agriculturalstocks and raw materials like corn rice wheat cassava sugarcane sugar beet and sweet sorghum through biochemical orthermochemical processes [161793] Even though the route ofproduction depends on the raw material it can be summarized asthe breaking of the biomaterial to simple sugars that furtherfermented using alcohol producing microorganisms The producedethanol later separated and concentrated through downstreamprocesses (Fig 4)

Facing the conflict of global energy and food demand therehave been increasing interest and worldwide studies in producingbioethanol from alternative sources like microalgae rather thanfeedstock that has minor impact in the daily life [161793]

Bioethanol from microalgae can be produced through thefermentation of the microalgal biomass or directly through cellularreactions [9495]

When considering ethanol production via fermentation the keyis the accumulation of starch which is a potential substrate thatcan reach half of the microalgas cellular dry biomass Microalgalstarch can be extracted by mechanical or enzymatic means andfurther separated by downstream processes incorporating wateror an organic solvent This starch will be hydrolyzed to glucose tobe used in ethanol fermentation [9697] Production mainly differsfrom other crop raw materials in the first steps of the processbecause microalgae will need special concentration harvestingand mechanical disruption systems related with their cellularphysiology and culturing [98]

Microalgae can also excrete ethanol directly through the cellwalls by means of intracellular processes under dark becauseillumination prevents the formation of ethanol except for minoramounts This process which is reported in some microalgae likeChlorococcum littorale [99] Chlamydomonas reinhardtii [8384]Chlamydomonas moewusii [100] Chlorella vulgaris [101] Oscilla-toria limnetica [102] Oscillatoria limosa [99] Gleocapsa alpicola[103] Spirulina platensis [68] Cyanoteche sp [99] covers theanaerobic metabolism in algae where the assimilation and forma-tion of hydrogen carbon dioxide formate acetate ethanol lactateglycerol and butannediol take place [1783] Degradation of intracel-lular starch which is the main endogenous carbon source storedduring aerobic phototrophic metabolism to pyruvate is accomplishedby the EmbdenndashMeyerhofndashParnas and pentose phosphate pathwaysusing pyruvate decarboxylase and alcohol dehydrogenase enzymes[99102] As stated by Gfeller and Gibbs [83] the lack of ethanolproduction by the microalgae cells during illumination is related withthe absence of available reduced pyridine nucleotides with theassumption of active acetaldehyde and alcohol dehydrogenases Twopossible conversion routes for acetyl-CoA to acetate and ethanol canbe followed In the former route half of the acetyl-CoA is converted toacetate by a deacylase while the rest is reduced to ethanol withacetaldehyde as intermediate In the latter route acetyl-CoA is reducedto acetaldehyde that undergoes a dismutation sequence until theformation of acetate and ethanol [8384]

Enhancing direct microalgal bioethanol production by geneticmanipulations is also under consideration Genes from the ethanolproducing bacterium Zymomonas mobilis was transfered intomicroalgae Synechococcus sp aiming to give the ability to utilizethe fixed carbon for direct ethanol excretion to the culture volumethrough the cell walls [93104]

The novelty of the process lies in the separation of producedbioethanol from the culture medium This process eliminates theharvesting step that decreases the energy costs and water usageassociated with the separation processes required for algae har-vesting and fuel extraction [94105]

Besides bioethanol being the main product the remainingmicroalgal biomass may be used to produce biomethane again

Table 4Microalgal hydrogen production

Microalgae Cultivation Process PBR type Culture medium Hydrogen productionprocedure

Time H2 production Refs

Anabaena variabilis (CCAP 14034B)

Continuousndashphotoautotrophic

Lab Stirred (300 mL) Nitrogen free Allen-Arnon

Nitrogen free Allen-Arnon medium

Under vacuum for 15 min Increased light intensity for

5 h at the 6th day ofcultivation

35 days 12ndash14 mL gminus1DW hminus1 [164]

Anabaena variabilis (ATCC 29413) Continuousndashphotoautotrophic

Lab Vial (14 mL) Allen-Arnon(containing Na2MoO4 orNa3VO4 or neither)

Under argon flushing 80ndash100 h

Up to 5 nmol hminus1 mg Chlaminus1 at pH levels of 7ndash9 with Na3VO4 added cultures

[165]

Anabaena sp PCC 7120 (3hydrogenase mutants from PCC7120)

Batchndashphotoautotrophic Lab Sealed polystyrenecuvettes (1 cm light path47 mL capacity)

BG 11 Nitrogen free BG 11 medium Under anaerobic conditions Various light intensities

32ndash40 h Up to 08ndash1 mmol per cuvette (47 mL) [63]

Anabaena sp PCC 7120 and itsmutant AMC 414

Continuousndashphotoautotrophic

Outdoor Tubular-coiled (435 L) BG 11 Nitrogen free BG 11 medium Under argon atmosphere Nitrogen free BG 11 medium Under anaerobic conditions Increased light intensity

7 days 149 mL hminus1Lminus1PBR (373 mL total) with themutant

[166]

Anabaena variabilis (ATCC 29413) Batchndashphotoautotrophic Lab Panel (500 mL capacity) BG 11 50 h Up to 40ndash50 mL [167]

Chlamydomonas reinhardtii(CC124)

BatchndashphotomixotrophicSynchronous andunsynchronous growth

Lab Stirred glass bottles(12L)

TAP TAP-S medium (transferred bycentrifugation)

140 h 102 mL (with 4 h synchronizedcultures)

86 mL (with unsynchronized cultures)

[168]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotomixotrophic Lab Stirred glass bottles(500 mL)

TAP TAP-S medium transfer bycentrifugation

TAP-S medium inoculationby TAP culture (10inoculation)

175 mL Lminus1 (with centrifuged cultures under20ndash40 mE mminus2sminus1 average light intensity)

[87]

Chlamydomonas reinhardtii(CC124)

Continuousndashphotomixotrophic

Lab Stirred glass bottles(1050 mL)

TAP-S (90 mmol sulfateadded)

TAP-S medium two stagechemostat with aerobicstage and anaerobic stage

TAP-S medium TAP medium with limiting

sulfate (10ndash20 mM) Anaerobic conditions Sulfur free medium Anaerobic

4000 h Up to 058 mL hminus1Lminus1PBR [169]

Chlamydomonas reinhardtii (Dang137C mt+ and a nonmotilemutant CC 1036 pf18 mt+)

Batchndashphotomixotrophic-immobilized

Lab Panel (160 mL) TAP (046 mM sulfatereplete)

23 days 45 mL dayminus1 (380 mL total) [170]

Chlamydomonas reinhardtii (Dang137C mt+)

Batch-photoautotrophicmixotrophic andheterotrophic

Lab Flat glass bottles PBR(15 L volume)

HS (CO2 bubbling) TAPwith or without CO2

bubbling

60ndash80 h 11704 mmol Lminus1 (sim28 mL (hL)minus1) inphotoautotrophic cultures

45716 mmol Lminus1 (sim40 mL (hL)minus1) inphotoheterotrophic cultures

09708 mmol Lminus1 (sim69 mL (hL)minus1)inphotomixotrophic cultures

[171]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotoautotrophic Lab Flat glass bottles PBR(15 L)

High salt HS sulfur free medium Argon purging during the

first 24 h of deprivation TAP-S medium Various dilutions Anaerobic conditions

100 h 7173 mL Lminus1 (175 mE mminus2sminus1 lightintensity pH 77)

5272 mL Lminus1 (420 mE mminus2sminus1 lightintensity pH 74)

[172]

Chlamydomonas reinhardtii(CC124)

Semi continuousndashphotomixotrophic

Lab Stirred tank (25 L) TAP 127 days 1108 mL [173]

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic-immobilized

Lab Vials (75 mL) TAP TA-S-P (no sulfate nophosphate) medium

Alginate entrapped

160ndash180 h

0307002 mol mminus2 (125 mmol mgminus1 Chl hminus1) [174]

Batchndashphotomixotrophic Lab Glass bottles (325 mL) TAP 192 h 395 mmol106 cellsminus1 hminus1 with TAP-S [90]

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harvested cells flushed withor without argon

Anaerobic conditions TAP-S or TAP-N DCMU mixed ethanol

addition Dark anaerobic

fermentation

Chlamydomonas reinhardtii(CC124)

34 mmol106 cellsminus1 hminus1 with TAP-N

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Stirred tank (1 255 L) TAP-S TAP-S medium transfer bycentrifugation

Various mixing time Various light energy Scale-up

192 h Max with 122 kJ sminus1 mminus3 light energy and25 min mixing time

[202]

1 L PBR 1537005 mL Lminus1 hminus1

25 L PBR 1327005 mL Lminus1 hminus1

5 L PBR 1027005 mL Lminus1 hminus1

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Tubular (110 L) TAP-S TAP-S medium transfer bycentrifugation

Modified with silicananoparticle to enhancescattering

48 h 3121571789 mL (06 mL Lminus1 hminus1) [203]

Chlorella pyrenoidosa C-101 Batchndashphotoautotrophic Lab Bubble column (650 mL) Modified Bristol Nitrogen flushing under dark forldquo420rdquo h

60ndash65 h 6910minus2 m3 kgminus1 cell [65]

Chlorella vulgaris MSU 01 Batchndashphotomixotrophic Lab Stirred (500 mL) Modified BG11 and MJ Anaerobic conditions Corn stalk as carbon source

in the medium

6ndash7 days 26 mL [175]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Dark incubation Anaerobic nitrogen

atmosphere Addition of specific effectors

(DCMU DCCD DBMIBand CCCP)

Continuous illuminationafterwards

8 h 0339 mL hminus1 Lminus1 (144 mL) based on1106 cells mLminus1 at 15 μM CCCP addedculture after 8 h of illumination

[66]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Sulfur deprive medium Incubation under dark Anaerobic conditions Continuous illumination

afterwards

50 h 11720 nL hminus1 (with seawater-S medium) [67]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Torus (15 L) Defined mineral Dark incubation Anaerobic nitrogen

atmosphere 15 μM CCCP addition Continuous illumination

afterwards

4ndash6 days 720 mL hminus1 (2366770 mL) [176]

Platymonas helgolandica vartsingtaoensis

Batchndashphotoautotrophic Lab Jars (130 mL) F2 Anaerobic Illuminated -S medium Dark CCCPDCMU or both

added medium

25 h 0002 mmol Lminus1 withndashS medium 0160 mmol Lminus1 with CCCP medium 0014 mmol Lminus1 with DCMU medium 0290 mmol Lminus1 with CCCP

+DCMU medium

[89]

Spirulina platensis (NIES-46) Batchndashphotoautotrophic Lab Erlenmeyer flasks(60 mL)

SOT Nitrogen free medium Under dark

20 h 2 mmol mgDWminus1 [68]

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Table

4(con

tinu

ed)

Micro

alga

eCu

ltivation

Pro

cess

PBRtype

Culture

med

ium

Hyd

roge

npro

duction

pro

cedure

Time

H2pro

duction

Refs

Anae

robicco

nditions

Syne

chocystissp

PCC68

03an

dits

mutantNDH-1

complex

defi

cien

tM55

Batch

ndashphotoa

utotrop

hicndash

encapsu

lated

Lab

Vials

(2mL)

BG

11

Nitroge

natmosphere

Under

cycled

lightan

ddark

exposure

5day

s0005

ndash004

5mM

[177

]

Tetraspo

rasp

CU25

51Batch

ndashphotom

ixotrophic

Lab

Vials

TAP(w

itho

rwithou

t05mM

β-mercaptoethan

olfor

24h)

Su

lfuran

dnitroge

ndep

rive

dmed

ium

Argon

flush

edan

aerobic

atmosphere

424

h173ndash61

7mm

olmgminus

1Chlahminus1

[178

]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264252

through anaerobic digestion for electricity generation The carbondioxide and discharged water formed as by-products of thefermentation can be recycled for the microalgae cultivation tofulfill the biorefinery concept [94105]

24 Biomethane

Today agricultural plants or by-products are conventionalsources for renewable biogas production which is mainly amixture of methane (55ndash75) and carbon dioxide (25ndash45) byanaerobic digestion Biomethane from the biogas can be used as afuel for transportation and electricity generation or for heatingpurposes especially in the rural areas [16106107]

Microalgae with their dominancy over crop plants by means ofproductivity per hectare triggered the attention for the production ofbiogas The solar energy converted and stored by the microalgae cellsthrough photosynthesis can be transformed into energy through theanaerobic digestion to produce methane [106108]

Microalgal biomass having high cellular lipid starch andprotein low cellulose and on the other hand the absence of ligningives a reliable and effective anaerobic digestion These specifica-tions make microalgae a good alternative for effective biomethaneproduction compared to the other crop plants [16107108]

Microalgal biomass can be processed anaerobically step by stepwith specialized groups of bacteria [109]

Hydrolyzation of biopolymers to monosaccharides by hydro-lytic bacteria

Fermentation of the monosaccharides to carboxylic acids andalcohols by fermentative bacteria

Conversion of the acids and alcohols to acetate hydrogen andcarbon dioxide by acetogenic bacteria

Conversion of the end products of acetogenic reactions tomethane and carbon dioxide by methanogenic bacteria

Microalgal biomass remaining after the anaerobic digestion canbe further processed to make fertilizers that can add an extra valueto the overall process Also the carbon dioxide portion of theproduced biogas can be recycled again to cultivate the neededmicroalgal biomass for processing [107110ndash112]

A predicted model of microalgae biomass for digestion toproduce electrical and thermal energy discussed the economicprofitability related with technical aspects of the productionsystem The results showed that the microalgae productivityharvesting concentration and usage of high rate anaerobic diges-ters are the key factors for the economic energy production [113]

A life cycle perspective study using a stochastic model indi-cated that when compared with the conventional crops likeswitch grass canola and corn the environmental impact ofmicroalgal biomass production is higher with respect to energydemand greenhouse gas emissions and water use regardless ofcultivation location Only in overall land use and eutrophicationpotential microalgae present favorable results [114] This mayseem to be a disadvantage to produce biomethane from microalgalbiomass but the studies also supported that the integratedprocesses using proper photobioreactors combining microalgaecultivation and waste water treatment systems for biomethaneproduction will help to reduce the environmental impacts result-ing in a competitive and effective production [11416115]

25 Integrated processes

Relations between parameters and the target products (bio-mass lipid hydrogen ethanol) are important in the selection ofthe microalgae for efficient biofuel production As can be followedfrom the tables summarizing the microalgal biofuel productions

Sugars

- Sugarcane juice

- Molasses

- Sugar beet

Starch

- Corn

- Oats

- Wheat

- Sago Palm

- Cassava

- Banana wastes

- Rye

- Barley

- Triticale

- Sorghum

- Algal biomass

Lignocellulosic materials

- Crop residues

- Cellulose wastes

- Hardwood

- Harbaceous biomass

- Softwood

- Municipal solid wastes

Fermentation

- Saccharomyces cerevisiae

- Schizosaccharomyces pombe

- Zymomonas mobilis

- Saccharomyces bayanus

- Pichia stipitis

- Candida shehatae

- Pachysolen tannophilus

- Mucor indicus

- Chalara parvispora

- T thermosaccharolyticum

- T Ethanolicus

- B Stearothermophilus

- C thermohydrosulfuricum

- C thermocellum

- Milling

- Grinding

- ShredingBreaking hemicellulose

chains

- Physical

- Chemical

- Physicochemical

- Biological

Hydrolization -Detoxification

-Neutralization

Sugars

- Hexoses

- Pentoses

Separation and

Concentration

- Distillation

- Rectification

- Dehydration

ETHANOL

Fig 4 Ethanol production from biomass productionSource Adapted from Refs [9398201]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 253

studies focus on the separation of production processes into twomain steps growth mediated and product mediated When con-sidering direct biofuel production the main approach is product

mediated for higher lipid hydrogen or ethanol production Whenconsidering biofuel production integrated with other microorgan-isms (Table 5) the main approach is growth mediated for higher

Table 5Integrated biofuel processes working with microalgae

Microalgae System Product Ref

Chlamydomonas reinhardtii (UTEX 90) Enzymatic treatment of algal biomass and conversion to ethanol by Saccharomyces cerevisiae Ethanol [179]Chlamydomonas reinhardtii (UTEX 90) Hydrothermal acid treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [180]Chlorella vulgaris (IAM C-534) Enzymatic treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [181]Synechococcus leopoliensis (IAMM 6) Fermentation of acid treated saccharified algal biomass by yeast Saccharomyces sake (IFO 2347) Ethanol [97]Chlamydomonas reinhardtii Chlorella vulgaris (macroalgae Undaria pinnatifida) Enzymatic treatment of pre-acid hydrolyzed algal biomass fermentation by 4 different strains of Escherichia coli Ethanol [182]Schizocytrium sp Fermentation of hydrothermal treated algal biomass by E coli KO11 Ethanol [183]Microcystis aeruginosa and Anabaena variabilis Hydrolysis and fermentation of Super Critical fluid pretreated algal biomass by Saccharomyces cerevisiae Ethanol [204]Scenedesmus obliquus Fermentation of algal biomass hydrolysate by Kluyveromyces marxianus IGC 2671 Saccharomyces carlsbergensis

ATCC6269 and Saccharomyces bayanusEthanol [205]

Anabaena sp PCC7120 Fermentation of hydrogen produced residual algal biomass by Enterobacter aerogenes Hydrogen [184]Arthrospira (Spirulina) platensis Nannochloropsis sp and Dunaliella tertilecta Anaerobic fermentation of thermal pretreated algal biomass by immobilized Clostridium acetobutylicum Hydrogen acetone

ethanol butanol[206]

Chlorella vulgaris ESP6 Dark fermentation of acid or alkalineenzyme pretreated algal biomass hydrolysate by Clostridium butyricumCGS5

Hydrogen [207]

Chlorella sp Simultaneous hydrolysis and fermentation of algal biomass by sewage sludge consortia Hydrogen [208]Thalassiosira weissflogii Dark fermentation of algal biomass with the thermophilic bacterium Thermotoga neapolitana Hydrogen [209]Chlamydomonas reinhardtii (IAM C-238) Chlorella pyrenoidosa (IAM C-212) andDunaliella tertiolecta (ATCC 30909)

Fermentation of algal biomass by Lactobacillus amylovorous (ATCC 33620) and Rhodobacter sphaeroides RV Hydrogen [185]

Chlamydomonas reinhardtii (IAM C-238) and Dunaliella tertiolecta (ATCC 30909) Fermentation of algal biomass by Lactobacillus amylovorous and Rhodobium marinum (A-501) mixed culture Hydrogen [186]Chlamydomonas (MGA 161) Fermentation of algal biomass by Rhodovulum sulfidophilum (W-1S) Hydrogen [85]Chlamydomonas reinhardtii (C238) Mixed cultivation of Chlamydomonas reinhardtii (C238) with Rhodospirillum rubrum (NCIB 8255) Hydrogen [187]Scnedesmus sp Fermentation of algal biomass by anaerobic digested sludge Hydrogen [188]Arthrospira maxima Anaerobic digestion of algal biomass by sewage sludge consortia Methane [210]Phaeodactylum tricornutum Anaerobic digestion of algal biomass by potato factory origin anaerobic granular sludge Methane [211]Scenedesmus sp Anaerobic digestion of high pressure thermal pretreated raw and residue (from lipid extraction) algal biomass

and by anaerobic digestor sludgeMethane [212]

Scenedesmus sp Anaerobic digestion of ultrasound and thermal pretreated raw algal biomass by sugar factory origin anaerobicgranular sludge

Methane [213]

Scenedesmus sp Anaerobic digestion of mild thermal pretreated raw algal biomass by sugar factory origin anaerobic granularsludge

Methane [214]

Spirulina platensis Anabaena variabilis and Chlorella sp Processing of algal biomass by an integrated system of methanogenic culture and Rhodobacter capsulatus Methane and hydrogen [189]Spirulina platensis (UTEX 1926) Rhodotorula glutinis (2541) Mixed cultivation of microalgae and yeast using waste water Lipid (biodiesel) [190]Spirulina platensis Using excess CO2 from the ethanol fermentation by Saccharomyces cerevisiae Lipid (biodiesel) [119]Botryococcus braunii (two strains BB763 and BB764) Chlorella vulgaris Chlorellapyrenoidosa

Biodiesel production catalyzed by immobilized Penicillium expansum lipase and Candida antarctica lipase B(Novozym 435)

Lipid (biodiesel) [191]

Chlorella vulgaris (21111B) Anaerobic digestion of algal biomass by sewage sludge origin methanogenic culture Methane [112]Chlorella sp and Scenedesmus Anaerobic digestion of algal biomass by sewage sludge culture Methane [106]Chlorella sp Anaerobic digestion of algal biomass by sludge culture Methane [192]Arthrospira platensis Chlamydomonas reinhardtii Chlorella kessleri Dunaliellasalina Euglena gracilis and Scenedesmus obliquus

Anaerobic digestion of algal biomass by sewage sludge culture Methane [107]

Spirulina maxima Anaerobic digestion of algal biomass by sewage sludge culture Methane [193]Chlorella sp and Scenedesmus Anaerobic codigestion of algal biomass with waste paper by methanogenic culture Methane [194]Tetraselmis Anaerobic digestion of algal biomass by methanogenic culture Methane [195]Chlorococcum sp Anaerobic treatment of distillery waste with algal biomass by acidogenicmethanogenic culture Methane [196]Phaeodactylum tricornutum (CCAP10551) Anaerobic digestion of algal biomass by granular seed sludge from digester treating potato processing waste

water dominated by Methanosaeta sp and Methanosarcina spMethane [197]

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 255

biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264256

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

SSOncel

Renew

ableand

SustainableEnergy

Review

s26

(2013)241

ndash264258

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 259

technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

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[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264262

[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 4: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

MIC

RO

ALG

AE

Oil Extraction

Hydrotreatment Green Diesel

Transesterification Biodiesel

Fermentation

Ethanol

Hydrogen

Gasification Syngas

Fermentation

Ethanol

Butanol

Butyric Acid

Acetic Acid

Methane

Methanetion Methane

Hydrogen

Anaerobic Digestion Methane

Biophotolysis Hydrogen

Pyrolysis

Bio-oil

Syngas

Charcoal

Fig 2 Biofuel routes from the standpoint of microalgaeSource Adapted from Refs [816108199]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264244

of triacylglycerols which are actually the key component of algallipids for biodiesel production Triacylglycerols are distinct frommembrane glycerolipids because of their character as the storagematerial for energy instead of structural usage [913]

Lipid productivity of a microalga is accepted to be an indicatorof its potential for biodiesel production

Studies focus on different parameters such as nutrient sourcenutrient concentration light intensity salinity pH mixing speed andtemperature to enhance the lipid productivity of the microalgae(Table 3) Microalgae show variable responses to the effects resultingin various lipid productivities For example on cultivation with 10CO2 biomass productivity of the Scenedesmus sp was higher thanBotryococcus branuii on the other hand lipid productivity was lowerbut similar productivities could be seen in the case of flue gas(55 CO2) cultivation [14] In another study results indicated thatpotassium phosphate and magnesium sulfate are the major mediacomponents affecting the lipid productivity of Botryococcus branuiiand the lipid and biomass optimized media should differ in concen-trations [15] The key is to select the proper method of approachconsidering the microalga for the lipid productivity

Extraction of microalgal lipids is the bottleneck for high yield inproductions After the harvest the culture starts its downstreamjourney As a first step the excess water that is an unwantedvolumetric load is removed through concentration processes likefiltration drying flocculation and centrifugation The concentratedcells can either be extracted directly or through a disruption stepin which the intercellular content was released to enhance theextraction process Considering microalgae because the targetproduct oil is trapped inside strong cell walls the disruption stepcan be termed as a part of the extraction step [16ndash18] Microalgaloils could be extracted using milling expeller press high pressurehomogenization solvent enzyme supercritical fluid osmoticshock pulsed electric field microwave or ultrasound techniquesThe selection of the method depends on the specie cost andefficiency as well as the environmental concerns The extractedlipids then passed to the fractionation step where the undesiredpolar lipids and non-acylglycerol neutral lipids (such as free fattyacids hydrocarbons sterols ketones carotenes and chlorophylls)were removed Later the purified product is converted intobiodiesel through the transesterification process [19ndash24]

Table 3Various studies focusing on lipid productivities as the key element for biodiesel production

Microalgae Effect Time Cultivation PBR type Lightintensity(lE mminus2 sminus1)

Temp(1C)

Medium Maximum production Ref

Botryococcus braunii(UTEX 572)

CO2 14 days Batchndashautotrophic Bubble column 150 2571 Modified Chu 13 5517153 mg Lminus1 dminus1 (21 biomass) with10 CO2 enriched air

2065 mg Lminus1 dminus1 (24) with 55 CO2

containing flue gas

[14]

Botryococcus braunii(765)

CO2 28 days Batchndashautotrophic Airlift (3 L) 150710 25 Modified BG11 1174 mg Lminus1dminus1 (12717083 biomass) with20 CO2 enriched air

[143]

Botryococcus braunii(UTEX 572)

Media components 18 days Batchndashautotrophic Bubble column(06 L)

50 22 Modified BG11 019 g Lminus1 dminus1 (6496 biomass) in lipidoptimized media

018 g Lminus1 dminus1 (5956 biomass) in growthoptimized media

[15]

Botryococcus braunii(KMITL 2)

Light intensity light cycle nitrogenphosphorus iron cultivation time salinity

40 days Batchndashautotrophic Flasks (1 L) 0ndash538(LD cycle)

25 Chlorella 54697313 with 200 mE mminus2 sminus1 continuouslight 222 mg Lminus1 phosphorus and a salinity of0 psu

[144]

Chlamydomonasreinhardtii

pH and CO2 31 days Batchndashautotrophic BIOCOIL (15 L) 220 2571 Artificial or wastewater

05057002 g Lminus1 dminus1 (2525 biomass) with 33CO2 at pH 75

[145]

Chlorella vulgaris(CCAP 211)

Temperature nitrogen concentration andextraction techniques

14 day Batchndashautotrophic Erlenmayer flask(2 L)

70 15ndash25 Guillard F2 20227060 mg Lminus1 dminus1 (14717030) at25 1C

20307040 mg Lminus1 dminus1 (15317051) with0375 g Lminus1 nitrogen concentration

[146]

Chlorella sorokiniana(GXNN01)

Carbon sources and concentrations 70 h Batchndashautotrophicheterotrophic

Erlenmayer flask(015 L)

0ndash80 3072 BBM 028870008 g Lminus1 (028770018 g gDWminus1)with acetate

Glucose concentration of 20 mmol Lminus1 gavethe maximal lipid yield

0048 lipid gminus1DW dayminus1 (232) inmixotrophic perfusion (rate 28 L hminus1)culture

[147]

Chlorella minutisima(UTEX LB-2341)

Long term outdoor production 80 days Batch or perfusionautotrophicndashmixotrophic

Cylindrical vessel(20 L10 200 Ltotal)

0ndash700 30ndash35 Enriched sea water [148]

Chlorellaprotothecoides(UTEX 249)

Carbon source concentration nitrogenconcentration salinity pH level andagitation speed

103 h Batchndashautotrophicmixotrophicheterotrophic

Erlenmeyer flasks(01 L)

8W 26 Modified basal 025 g Lminus1 dminus1 (25257007) with 15 g Lminus1

glucose 69 pH 019 g Lminus1 dminus1 (20337513) with 204 gLminus1

glycerol 71 pH 0177001 g Lminus1 dminus1 (23087318) with

205 g Lminus1 acetate 67 pH

[149]

Chlorellaprotothecoides(SAG 3380)

CO2 14ndash15days

Batchndashautotrophicmixotrophic

Erlenmeyer flasks(025 L)

100710 2471 BG11 with Peptone 213725 DW (Mixotrophic 1 glycerol) 115731 DW (Autotrophic) 358715 DW (Mixotrophic N-deprived)

[150]

Chlorella pyrenoidosa Waste water 10 days BatchndashMixotrophic Flasks (01 L) 63 25ndash27 Diluted piggery wastewater

(with 1000 mg Lminus1 COD) [151]

Chlorella pyrenoidosaFACHB-9

Waste water 120 h Batchfedbatchndashmixotrophic

Flasks (05 L) 405 (1410LD cycle)

2771 Soybean process wastewater

04 g Lminus1 dminus1 (377934 DW) with fed batchculture

[152]

AuxenochlorellaprotothecoidesUMN280

CO2 waste water 12 days Batchndashmixotrophic Roux bottles(058 L)

60 2572 Waste water (05 L)and BG11 seed culture(008 L)

0182 g Lminus1 (1866 DW) without CO2

0418 g Lminus1 (2082 DW) with 1 CO2

0516 gLminus1 (2058 DW) with 5 CO2

[153]

Chlorella vulgaris KNO3 CO2 and light intensity 250 h Batch 24ndash120 25 Artificial sea water [154]

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Table 3 (continued )

Microalgae Effect Time Cultivation PBR type Lightintensity(lE mminus2 sminus1)

Temp(1C)

Medium Maximum production Ref

Membrane spargedcylindrical vessel(5 L)

40 mg Lminus1 dminus1 (20) at 60 mE mminus2sminus1 lightintensity 1 mM KNO3 concentration 1 CO2

enrichmentChlorellavulgarisKCT-CAG10032

CO2 14 days Batchndashautotrophic Bubble column 150 2571 BG11 6917003 mg Lminus1dminus1 (7 biomass) with 10 CO2

enriched air[14]

Chlorella vulgarisBEIJ-H14

Glucose and urea 665 h Fed batchndashheterotrophic

Stirred tank (600 L) Dark 36ndash37 Glucose enrichedmedium

97 dry weight [155]

Chlorella vulgarisCCALA 256

Nutrient limitation 8 days Batchndashautotrophic Thin layer (150 L) 100ndash960 195ndash33

14 SS 032670010 g Lminus1 dminus1 (306705 DW) [156]

Choricystis minor Temperature dilution rate andpostharvest methods

Continuousndashautotrophic

Stirred tank (4 L) 550 10ndash30 BG 11 82 mg Lminus1 dminus1 (213717) at 25 1C and adilution rate of 0014 hminus1

Lipid content increased up to 595716under postharvest conditions withoutphosphate and nitrate

[157]

Nannochloropsisoculata

Temperature nitrogen concentration andextraction techniques

14 days Batchndashautotrophic Erlenmayer Flask(2 L)

70 25ndash38 BBM 9117030 mg Lminus1 dminus1 (14927082) at15 1C

16417011 mg Lminus1 dminus1 (15867059) with0075 gLminus1 nitrogen concentration

[139]

Nannochloropsisoculata

Temperature nitrogen and yeast extractconcentrations

16 days Batchndashphotomixotrophic

Airlift (2 L) 160ndash270 15ndash35 F2 10ndash15 (50 ppm nitrogen) 20-25 (125 ppm nitrogen) 25ndash30 (15 1C) 20ndash25 (35 1C)

[158]

Haematococcuspluvialis

Continuous light intensity or light cyclesno nitrogen or no aeration on production

14 days Batchndashautotrophic Flask 90 24 BBM 15617146 DW Under normal conditions 34857078 DW Under full medium

continuous light with aeration 32997277 DW Under continuous light

aeration no nitrogen

[159]

Neochlorisoleoabundans(UTEX-1185)

Nitrogen sources and concentrations 7 days Batchndashautotrophic Bubble column(1 L)

360 3072 SE 0133 g Lminus1 dminus1 (38) with 5 mM sodium nitrateas nitrogen source

[160]

Neochlorisoleoabundans(UTEX-1185)

Temperature CO2 and nitrate 18 days Batchndashautotrophic Bubble column(1 L)

150 26ndash30 BM 56 biomass with nitrogen starvation at 30 1Ctemperature without CO2 in air

[161]

Neochlorisoleoabundans(UTEX-1185)

Nitrogen starvation 140 h Continuousndashautotrophic

Flat panel airlift(1 L)

270 25 BBM 126 g mminus3 dminus1 (23) continuous culture withno mineral limitation with nitrate starvation

20657013 mg Lminus1dminus1 (9 biomass) with10 CO2 enriched air

3944 mg Lminus1 dminus1 (18) with 55 CO2

containing flue gas 16ndash18 DW with nitrogen deplete two stage

process 10ndash12 DW with single stage process

[162]

Scenedesmus spKCTC AG20831

CO2 14 days Batchndashautotrophic Bubble column 150 2571 BG11 [14]

Tetraselmis suecica Light and nitrogen concentration 9 days Batchndashautotrophic Stirred tank (20 L) 363ndash1331 2071 Modified F2 [163]

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 247

The preferred route for biodiesel production from oils istransesterification rather than pyrolysis and micro-emulsionbecause of the cost and quality concerns [25] Transesterificationis simply the reaction between triacylglycerols and an acyl-acceptor which can be carboxylic acids (acidolysis) alcohols(alcoholysis) or another ester (interesterification) [2526] Biodie-sel production from microalgal oils through transesterificationprocess has several steps (Fig 3)

The reaction can be chemically (acid or base) or biologically(enzyme) catalytic or non-catalytic (high pressure process) [27ndash29]

Homogeneous (NaOH CH3ONa KOH KOCH3) and heterogeneous(alkaline earth metal oxides zeolite KNO3 loaded on Al2O3 KNO3Al2O3 BaO SrO CaO MgO) base catalysts are conventionally used forbiodiesel production They are more effective with an oil having free

Strain selection

- Determination of cell culture condition

- Optimization of lipid production conditions

- Scale -up

Photobioreactor

LightCO2 Nutrients

Separation amp

Refining

Acid Water

CatalystAlcohol Glycerol

Temperature

Fig 3 Microalgal biodiesel productionSource Adapted from Refs [7 4647199200]

fatty acid concentration up to 2 resulting in high reaction rates(4000 faster) and conversion efficiency under lower operationtemperatures compared to acid catalysts But considering watercontent and acidity of the biodiesel feedstock acid catalysts arepreferred to prevent saponification Even if acid catalysts are effectivewith non-edible oils their limitations like the need for higher amountsof alcohol higher temperatures and pressures slower reaction ratesresult in lower yields Both homogeneous and heterogeneous acidcatalysts (sulfuric acid hydrochloric acid phosphoric acid and sulfo-nated organic acids) are used especially in two step biodiesel produc-tion where in the first step the oil reacts with alcohol by acid catalystsand later reacted with the base catalyst This procedure is preferredwith high free fatty acid concentrated oils where the proceduredecreases the value of the free fatty acids to operational levels [1030]

Water

Biomass Harvesting

- Filtration

- Centrifugation

- Sedimentation

- Flotation

Dryer

Oil Extraction

-Chemical

-Biochemical

-Mechanical

Catalyst

-Chemical

-Biological

Oil

Alcohol

Transesterification

Biodiesel

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264248

Conventional technology of chemical catalysis has some con-straints due to the environmental problems related with soapformation and energy demand due to the downstream processesto recover glycerol and catalysts [262831]

Biological catalysis has some advantages over the chemicalcatalysis including lower energy demand moderate reaction con-ditions lower alcohol to oil ratio easier product recovery and highconversion [3132]

Lipases are the key biocatalysts that are used in biodieselproduction Major producer microorganisms for lipases are Aspergil-lus niger Aspergillus oryzae Bacillus pumilis Burkholderla cepaciaCandida antarctica Candida cylindracea Candida lipolytica Candidaparalipolytica Candida rugosa Chromobacterium viscosum Enterobac-ter aerogenes Eremothecium ashbyii Escherichia coli Geotrichumcandidum Mucor miehei Penicillium cyclopium Penicillium expansumPenicillium restrictum Pseudomonas cepacia Pseudomonas fluorescensPseudomonas fragi Rhizopus arrhizus Rhizopus delemar Rhyzomucormiehei Rhizopus oryzae Saccharomyces cerevisiae and Thermomyceslanuginosus which are also commercially important to meet theneeds of the large scale biodiesel processes [3334]

Main bottlenecks of this process include high cost of enzymelow yield due to inactivation longer reaction time slower reactionrate and the amount of water and organic solvents in the reactionmixture [2532]

The limitations in the biocatalysis are managed via the immo-bilization of the lipases in packed bed reactors to prevent washoutand inactivation [35] using whole cell immobilization [26] ionicliquids in enzyme catalysis [3136] genetic modifications andrecombinant microorganisms to enhance the efficiency and theproduction of the enzyme [26] alternative acyl acceptors [37]stepwise processes [3839] moderate polar solvents [40] non-catalytic methods under supercritical conditions [4142] and highpressure processes to stabilize the enzymes [4344]

From the economical point of view which is also importantchemical catalysis is reported to be cheaper than biologicalcatalysis But the modifications like using immobilized biocatalystsand the enhanced reuse can serve a competitive cost compared tothe chemical catalysts [45]

Numerous approaches are still in progress for the optimizationof the biodiesel production process adaptable to different feedtypes compositions and downstream requirements One of thenovel processes mentioned in recent studies is the ldquoMcgyan Processrdquothat consists of a continuous fixed bed reactor that can producebiodiesel using a metal oxide based catalyst The process is analternative method for continuous transesterification and can use awide variety of feedstock does not consume the catalyst reducesthe reaction time from hours to seconds and does not use water ordangerous chemicals [164647] Treatment of the lipids extractedfrom Dunaliella tertiolecta and Nannochloropsis oculata with Mcgyanprocess to produce biodiesel reached up to 85 in the conversion oftriacylglycerides and free fatty acids to alkyl esters [48]

Alternatively by shifting the production route microalgal oilscan be used to produce ldquogreen dieselrdquo by a process known ascatalytic hydroprocessing The basic difference of this with trans-esterification is the usage of hydrogen rather than the alcohol Alsothe by-products like propane water and carbon dioxide differfrom glycerol of transesterification [816] Green diesel has super-iority over biodiesel with its lower oxygen constitution similar tothe petroleum derived fuels with a near zero oxygen content Theprimary goal of the processes is to produce a minimized oxygencontaining green diesel with maximized final energy content[816] Also because of the high paraffinic hydrocarbon contentgreen diesel has higher cetane numbers and energy content onmass basis compared to biodiesel Using the microalgal oils forgreen diesel will be advantageous because of the applicationpotential in the conventional petroleum refinery systems with

existing infrastructure and the by-products (H2O and CO2) can berecycled to be used in the microalgae cultivation again

With the rapid progress in the area of genetic engineering theresearchers can now present the genome sequences of microalgaefor example a lipid producing microalgae specie that has potentialin biofuel production ie Nannochloropsis gaditana genome isnewly finalized and may become a model organism like Chlamy-domonas reinhardtii Chlorella variabilis Micromonas pusila Ostreo-coccus tauri Ostreococcus lucimarinus Thalassiosira psudonanaEmiliana huxleyii Fragilariopsis cylindrus Aerococcus aophageffe-rens Cyanidioschyzon merolae and Phaeodactylum tricornutum withcompleted genomes [4950] By understanding these model micro-organisms in molecular basis we can have the chance to improveproductivities in future applications

The ultimate idea was the excretion of the oils from themicroalgae cells without the need of extraction step This ideawas supported with the studies focusing on Escherichia coli andSaccharomyces cerevisiae to excrete lipids through membraneswith genetic engineering tools [5152]

22 Biohydrogen

Hydrogen with its unique properties is accepted to be arenewable sustainable and environmentally friendly energy car-rier that serve as one of the most promising alternative solution toovercome the growing environmental concerns considering thefuture energy demands [5354]

Today there are various conventional as well as novel strategiesto produce hydrogen from fossil fuels (steam reforming plasmareforming thermal cracking gasification) biomass (pyrolysismicrobial conversion syngas conversion supercritical conversiongasification) and water (photolysis thermolysis electrolysis)incorporating chemical and biological processes [272955] Evenif the hydrogen production is dominated by the chemical pro-cesses using fossil fuels biological processes started to get moreattention since the first studies in the 1920s [56ndash58]

The metabolic routes for biohydrogen production differ accord-ing to the microorganism [2759]

Microalgae

(a) Direct photolysis 2H2O-light-2H2+O2

(b) Indirect photolysis(1) 12H2O+6CO2-light-C6H12O6+6O2

(2) C6H12O6+12H2O-12H2+6CO2Photosynthetic bacteria(a) Photofermentation CH3COOH+2H2O-light-4H2+2CO2

(b) Water-gas shift CO+H2O-H2+CO2Anaerobic bacteria Dark fermentationC6H12O6+2H2O-4H2+2CO2+2CH3COOH

Related with their photosynthetic productivity and light utili-zation efficiency microalgae can perform special biochemical andphotochemical reactions with minimum requirements that makehydrogen production possible under aerobic and anaerobic envir-onments [60ndash62]

Microalga like Anabaena sp [6364] Chlorella pyrenoidosa [65]Chlorella vulgaris [66] Platymonas subcordiformis [6667] Spirulinaplatensis [68] and especially Chlamydomonas reinhardtii [6970] getattention in biohydrogen production

Microalgae use two classes of oxygen sensitive metalloenzymesnitrogenases and hydrogenases that are closely related with thefinal biohydrogen generation process in photosynthesis [6371]

There are several types of hydrogenases like the hup-encodedNiFe-uptake hydrogenases hox-encoded NiFe-bidirectional hydro-genases FeFe hydrogenases NiFeSe-bidirectional hydrogenases

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 249

and Fe-only hydrogenases utilized by bacteria and microalgae Onthe other hand nitrogenases of purple non-sulfur bacteria andheterocyst microalgae can be classified by their metal cofactor asmolybdenum iron and vanadium types [7273]

Nitrogenase is the part of the biological nitrogen fixation andhydrogenase is capable to catalyze hydrogen consuming reactionsBiohydrogen production based on these enzymes differs in energyconsumption Hydrogenase mediated reactions are about threetimes more efficient than nitrogenase catalyzed reactions based onspent energy in the form of ATP On the other hand nitrogenasesare relatively less sensitive to oxygen compared to hydrogenases[74ndash76] Relatively or not because both enzymes are sensitive tooxygen it is important to control culture conditions for optimalhydrogen production

Microalgal biohydrogen production can take place duringphotosynthesis from water by the two photosystems dark fer-mentation of the reduced carbon produced by photosynthesis andphotofermentation by the enzymatic oxidation of intracellularreductants derived from fermentation [77ndash80]

Even if the studies on microalgal biohydrogen started in the 1930s[568182] it was shown that the production can be achieved by theinactivation of photosynthetic water oxidizing activity catalyzed bythe reaction center of photosystem two (PSII) [83ndash85] the productiv-ities could not reach to meaningful levels until there was a novelprotocol depending on sulfur deprivation [69] This protocol dependson the succession of photosynthetic reactions in which oxygenproduction and carbon accumulation take place and anaerobic photo-reactions through which the consumption of stored photosyntheticcellular metabolites for biohydrogen generation take place Sulfurdeprivation triggers the conversion of PSII centers to an intermediatein the PSII repair cycle in other words from a QB-reducing to aQB-nonreducing form resulting in the decrease of photosyntheticoxygen evolution capacity [86ndash88]

Compared to the other methods like using inhibitors (DBMIBDCMU SAL C1-CCP etc) or alternating lightdark cycle the removalof sulfate from the growth medium achieves a reversible inactiva-tion with sustainable and increased hydrogen production [83ndash85]

Most of the recent studies focused on the two stage sulfurdeprivation protocol however as summarized by some of theexample studies from batch to continuous processes with variousprocedures the use of different microalgae is a good sign of theprogress towards the future (Table 4) But again some microalgaelike Platymonas subcordiformis Platymonas helgolandica or Chla-mydomonas moewusii are not sensitive to sulfur deprivation aswell as Chlamydomonas reinhardtii so utilization of inhibitors andnitrogen starvation enhance the hydrogen production [8990]

Also the outdoor studies point out another bottleneck in theproductions Even if the applications in lab scale are givingpromising results outdoor cultures still cannot reach the compar-able levels Microalgae cells have problems to tolerate the lightinhibition and sulfur deprivation when exposed to direct sunlightoutdoors They need to be acclimated to light before the hydrogenproduction phase [91]

Besides the studies on the enhancement of the biohydrogenproduction focusing on culture techniques like utilization of immobi-lized microalgae or stressed cultivations with regard to light andmedium components the progress in genetic engineering to improveproduction levels focuses on engineering truncated antennas of thespecies for better sunlight utilization outdoors without inhibition orengineering oxygen tolerant species that can produce hydrogen inaerobic conditions which is still under investigation [7392]

23 Bioethanol

Bioethanol may be considered as an alternative clean burningfuel because of its environmentally friendly combustion products

with low greenhouse gas effect relative to fossil fuels Todaycommercial bioethanol production is mainly from agriculturalstocks and raw materials like corn rice wheat cassava sugarcane sugar beet and sweet sorghum through biochemical orthermochemical processes [161793] Even though the route ofproduction depends on the raw material it can be summarized asthe breaking of the biomaterial to simple sugars that furtherfermented using alcohol producing microorganisms The producedethanol later separated and concentrated through downstreamprocesses (Fig 4)

Facing the conflict of global energy and food demand therehave been increasing interest and worldwide studies in producingbioethanol from alternative sources like microalgae rather thanfeedstock that has minor impact in the daily life [161793]

Bioethanol from microalgae can be produced through thefermentation of the microalgal biomass or directly through cellularreactions [9495]

When considering ethanol production via fermentation the keyis the accumulation of starch which is a potential substrate thatcan reach half of the microalgas cellular dry biomass Microalgalstarch can be extracted by mechanical or enzymatic means andfurther separated by downstream processes incorporating wateror an organic solvent This starch will be hydrolyzed to glucose tobe used in ethanol fermentation [9697] Production mainly differsfrom other crop raw materials in the first steps of the processbecause microalgae will need special concentration harvestingand mechanical disruption systems related with their cellularphysiology and culturing [98]

Microalgae can also excrete ethanol directly through the cellwalls by means of intracellular processes under dark becauseillumination prevents the formation of ethanol except for minoramounts This process which is reported in some microalgae likeChlorococcum littorale [99] Chlamydomonas reinhardtii [8384]Chlamydomonas moewusii [100] Chlorella vulgaris [101] Oscilla-toria limnetica [102] Oscillatoria limosa [99] Gleocapsa alpicola[103] Spirulina platensis [68] Cyanoteche sp [99] covers theanaerobic metabolism in algae where the assimilation and forma-tion of hydrogen carbon dioxide formate acetate ethanol lactateglycerol and butannediol take place [1783] Degradation of intracel-lular starch which is the main endogenous carbon source storedduring aerobic phototrophic metabolism to pyruvate is accomplishedby the EmbdenndashMeyerhofndashParnas and pentose phosphate pathwaysusing pyruvate decarboxylase and alcohol dehydrogenase enzymes[99102] As stated by Gfeller and Gibbs [83] the lack of ethanolproduction by the microalgae cells during illumination is related withthe absence of available reduced pyridine nucleotides with theassumption of active acetaldehyde and alcohol dehydrogenases Twopossible conversion routes for acetyl-CoA to acetate and ethanol canbe followed In the former route half of the acetyl-CoA is converted toacetate by a deacylase while the rest is reduced to ethanol withacetaldehyde as intermediate In the latter route acetyl-CoA is reducedto acetaldehyde that undergoes a dismutation sequence until theformation of acetate and ethanol [8384]

Enhancing direct microalgal bioethanol production by geneticmanipulations is also under consideration Genes from the ethanolproducing bacterium Zymomonas mobilis was transfered intomicroalgae Synechococcus sp aiming to give the ability to utilizethe fixed carbon for direct ethanol excretion to the culture volumethrough the cell walls [93104]

The novelty of the process lies in the separation of producedbioethanol from the culture medium This process eliminates theharvesting step that decreases the energy costs and water usageassociated with the separation processes required for algae har-vesting and fuel extraction [94105]

Besides bioethanol being the main product the remainingmicroalgal biomass may be used to produce biomethane again

Table 4Microalgal hydrogen production

Microalgae Cultivation Process PBR type Culture medium Hydrogen productionprocedure

Time H2 production Refs

Anabaena variabilis (CCAP 14034B)

Continuousndashphotoautotrophic

Lab Stirred (300 mL) Nitrogen free Allen-Arnon

Nitrogen free Allen-Arnon medium

Under vacuum for 15 min Increased light intensity for

5 h at the 6th day ofcultivation

35 days 12ndash14 mL gminus1DW hminus1 [164]

Anabaena variabilis (ATCC 29413) Continuousndashphotoautotrophic

Lab Vial (14 mL) Allen-Arnon(containing Na2MoO4 orNa3VO4 or neither)

Under argon flushing 80ndash100 h

Up to 5 nmol hminus1 mg Chlaminus1 at pH levels of 7ndash9 with Na3VO4 added cultures

[165]

Anabaena sp PCC 7120 (3hydrogenase mutants from PCC7120)

Batchndashphotoautotrophic Lab Sealed polystyrenecuvettes (1 cm light path47 mL capacity)

BG 11 Nitrogen free BG 11 medium Under anaerobic conditions Various light intensities

32ndash40 h Up to 08ndash1 mmol per cuvette (47 mL) [63]

Anabaena sp PCC 7120 and itsmutant AMC 414

Continuousndashphotoautotrophic

Outdoor Tubular-coiled (435 L) BG 11 Nitrogen free BG 11 medium Under argon atmosphere Nitrogen free BG 11 medium Under anaerobic conditions Increased light intensity

7 days 149 mL hminus1Lminus1PBR (373 mL total) with themutant

[166]

Anabaena variabilis (ATCC 29413) Batchndashphotoautotrophic Lab Panel (500 mL capacity) BG 11 50 h Up to 40ndash50 mL [167]

Chlamydomonas reinhardtii(CC124)

BatchndashphotomixotrophicSynchronous andunsynchronous growth

Lab Stirred glass bottles(12L)

TAP TAP-S medium (transferred bycentrifugation)

140 h 102 mL (with 4 h synchronizedcultures)

86 mL (with unsynchronized cultures)

[168]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotomixotrophic Lab Stirred glass bottles(500 mL)

TAP TAP-S medium transfer bycentrifugation

TAP-S medium inoculationby TAP culture (10inoculation)

175 mL Lminus1 (with centrifuged cultures under20ndash40 mE mminus2sminus1 average light intensity)

[87]

Chlamydomonas reinhardtii(CC124)

Continuousndashphotomixotrophic

Lab Stirred glass bottles(1050 mL)

TAP-S (90 mmol sulfateadded)

TAP-S medium two stagechemostat with aerobicstage and anaerobic stage

TAP-S medium TAP medium with limiting

sulfate (10ndash20 mM) Anaerobic conditions Sulfur free medium Anaerobic

4000 h Up to 058 mL hminus1Lminus1PBR [169]

Chlamydomonas reinhardtii (Dang137C mt+ and a nonmotilemutant CC 1036 pf18 mt+)

Batchndashphotomixotrophic-immobilized

Lab Panel (160 mL) TAP (046 mM sulfatereplete)

23 days 45 mL dayminus1 (380 mL total) [170]

Chlamydomonas reinhardtii (Dang137C mt+)

Batch-photoautotrophicmixotrophic andheterotrophic

Lab Flat glass bottles PBR(15 L volume)

HS (CO2 bubbling) TAPwith or without CO2

bubbling

60ndash80 h 11704 mmol Lminus1 (sim28 mL (hL)minus1) inphotoautotrophic cultures

45716 mmol Lminus1 (sim40 mL (hL)minus1) inphotoheterotrophic cultures

09708 mmol Lminus1 (sim69 mL (hL)minus1)inphotomixotrophic cultures

[171]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotoautotrophic Lab Flat glass bottles PBR(15 L)

High salt HS sulfur free medium Argon purging during the

first 24 h of deprivation TAP-S medium Various dilutions Anaerobic conditions

100 h 7173 mL Lminus1 (175 mE mminus2sminus1 lightintensity pH 77)

5272 mL Lminus1 (420 mE mminus2sminus1 lightintensity pH 74)

[172]

Chlamydomonas reinhardtii(CC124)

Semi continuousndashphotomixotrophic

Lab Stirred tank (25 L) TAP 127 days 1108 mL [173]

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic-immobilized

Lab Vials (75 mL) TAP TA-S-P (no sulfate nophosphate) medium

Alginate entrapped

160ndash180 h

0307002 mol mminus2 (125 mmol mgminus1 Chl hminus1) [174]

Batchndashphotomixotrophic Lab Glass bottles (325 mL) TAP 192 h 395 mmol106 cellsminus1 hminus1 with TAP-S [90]

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harvested cells flushed withor without argon

Anaerobic conditions TAP-S or TAP-N DCMU mixed ethanol

addition Dark anaerobic

fermentation

Chlamydomonas reinhardtii(CC124)

34 mmol106 cellsminus1 hminus1 with TAP-N

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Stirred tank (1 255 L) TAP-S TAP-S medium transfer bycentrifugation

Various mixing time Various light energy Scale-up

192 h Max with 122 kJ sminus1 mminus3 light energy and25 min mixing time

[202]

1 L PBR 1537005 mL Lminus1 hminus1

25 L PBR 1327005 mL Lminus1 hminus1

5 L PBR 1027005 mL Lminus1 hminus1

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Tubular (110 L) TAP-S TAP-S medium transfer bycentrifugation

Modified with silicananoparticle to enhancescattering

48 h 3121571789 mL (06 mL Lminus1 hminus1) [203]

Chlorella pyrenoidosa C-101 Batchndashphotoautotrophic Lab Bubble column (650 mL) Modified Bristol Nitrogen flushing under dark forldquo420rdquo h

60ndash65 h 6910minus2 m3 kgminus1 cell [65]

Chlorella vulgaris MSU 01 Batchndashphotomixotrophic Lab Stirred (500 mL) Modified BG11 and MJ Anaerobic conditions Corn stalk as carbon source

in the medium

6ndash7 days 26 mL [175]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Dark incubation Anaerobic nitrogen

atmosphere Addition of specific effectors

(DCMU DCCD DBMIBand CCCP)

Continuous illuminationafterwards

8 h 0339 mL hminus1 Lminus1 (144 mL) based on1106 cells mLminus1 at 15 μM CCCP addedculture after 8 h of illumination

[66]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Sulfur deprive medium Incubation under dark Anaerobic conditions Continuous illumination

afterwards

50 h 11720 nL hminus1 (with seawater-S medium) [67]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Torus (15 L) Defined mineral Dark incubation Anaerobic nitrogen

atmosphere 15 μM CCCP addition Continuous illumination

afterwards

4ndash6 days 720 mL hminus1 (2366770 mL) [176]

Platymonas helgolandica vartsingtaoensis

Batchndashphotoautotrophic Lab Jars (130 mL) F2 Anaerobic Illuminated -S medium Dark CCCPDCMU or both

added medium

25 h 0002 mmol Lminus1 withndashS medium 0160 mmol Lminus1 with CCCP medium 0014 mmol Lminus1 with DCMU medium 0290 mmol Lminus1 with CCCP

+DCMU medium

[89]

Spirulina platensis (NIES-46) Batchndashphotoautotrophic Lab Erlenmeyer flasks(60 mL)

SOT Nitrogen free medium Under dark

20 h 2 mmol mgDWminus1 [68]

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Table

4(con

tinu

ed)

Micro

alga

eCu

ltivation

Pro

cess

PBRtype

Culture

med

ium

Hyd

roge

npro

duction

pro

cedure

Time

H2pro

duction

Refs

Anae

robicco

nditions

Syne

chocystissp

PCC68

03an

dits

mutantNDH-1

complex

defi

cien

tM55

Batch

ndashphotoa

utotrop

hicndash

encapsu

lated

Lab

Vials

(2mL)

BG

11

Nitroge

natmosphere

Under

cycled

lightan

ddark

exposure

5day

s0005

ndash004

5mM

[177

]

Tetraspo

rasp

CU25

51Batch

ndashphotom

ixotrophic

Lab

Vials

TAP(w

itho

rwithou

t05mM

β-mercaptoethan

olfor

24h)

Su

lfuran

dnitroge

ndep

rive

dmed

ium

Argon

flush

edan

aerobic

atmosphere

424

h173ndash61

7mm

olmgminus

1Chlahminus1

[178

]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264252

through anaerobic digestion for electricity generation The carbondioxide and discharged water formed as by-products of thefermentation can be recycled for the microalgae cultivation tofulfill the biorefinery concept [94105]

24 Biomethane

Today agricultural plants or by-products are conventionalsources for renewable biogas production which is mainly amixture of methane (55ndash75) and carbon dioxide (25ndash45) byanaerobic digestion Biomethane from the biogas can be used as afuel for transportation and electricity generation or for heatingpurposes especially in the rural areas [16106107]

Microalgae with their dominancy over crop plants by means ofproductivity per hectare triggered the attention for the production ofbiogas The solar energy converted and stored by the microalgae cellsthrough photosynthesis can be transformed into energy through theanaerobic digestion to produce methane [106108]

Microalgal biomass having high cellular lipid starch andprotein low cellulose and on the other hand the absence of ligningives a reliable and effective anaerobic digestion These specifica-tions make microalgae a good alternative for effective biomethaneproduction compared to the other crop plants [16107108]

Microalgal biomass can be processed anaerobically step by stepwith specialized groups of bacteria [109]

Hydrolyzation of biopolymers to monosaccharides by hydro-lytic bacteria

Fermentation of the monosaccharides to carboxylic acids andalcohols by fermentative bacteria

Conversion of the acids and alcohols to acetate hydrogen andcarbon dioxide by acetogenic bacteria

Conversion of the end products of acetogenic reactions tomethane and carbon dioxide by methanogenic bacteria

Microalgal biomass remaining after the anaerobic digestion canbe further processed to make fertilizers that can add an extra valueto the overall process Also the carbon dioxide portion of theproduced biogas can be recycled again to cultivate the neededmicroalgal biomass for processing [107110ndash112]

A predicted model of microalgae biomass for digestion toproduce electrical and thermal energy discussed the economicprofitability related with technical aspects of the productionsystem The results showed that the microalgae productivityharvesting concentration and usage of high rate anaerobic diges-ters are the key factors for the economic energy production [113]

A life cycle perspective study using a stochastic model indi-cated that when compared with the conventional crops likeswitch grass canola and corn the environmental impact ofmicroalgal biomass production is higher with respect to energydemand greenhouse gas emissions and water use regardless ofcultivation location Only in overall land use and eutrophicationpotential microalgae present favorable results [114] This mayseem to be a disadvantage to produce biomethane from microalgalbiomass but the studies also supported that the integratedprocesses using proper photobioreactors combining microalgaecultivation and waste water treatment systems for biomethaneproduction will help to reduce the environmental impacts result-ing in a competitive and effective production [11416115]

25 Integrated processes

Relations between parameters and the target products (bio-mass lipid hydrogen ethanol) are important in the selection ofthe microalgae for efficient biofuel production As can be followedfrom the tables summarizing the microalgal biofuel productions

Sugars

- Sugarcane juice

- Molasses

- Sugar beet

Starch

- Corn

- Oats

- Wheat

- Sago Palm

- Cassava

- Banana wastes

- Rye

- Barley

- Triticale

- Sorghum

- Algal biomass

Lignocellulosic materials

- Crop residues

- Cellulose wastes

- Hardwood

- Harbaceous biomass

- Softwood

- Municipal solid wastes

Fermentation

- Saccharomyces cerevisiae

- Schizosaccharomyces pombe

- Zymomonas mobilis

- Saccharomyces bayanus

- Pichia stipitis

- Candida shehatae

- Pachysolen tannophilus

- Mucor indicus

- Chalara parvispora

- T thermosaccharolyticum

- T Ethanolicus

- B Stearothermophilus

- C thermohydrosulfuricum

- C thermocellum

- Milling

- Grinding

- ShredingBreaking hemicellulose

chains

- Physical

- Chemical

- Physicochemical

- Biological

Hydrolization -Detoxification

-Neutralization

Sugars

- Hexoses

- Pentoses

Separation and

Concentration

- Distillation

- Rectification

- Dehydration

ETHANOL

Fig 4 Ethanol production from biomass productionSource Adapted from Refs [9398201]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 253

studies focus on the separation of production processes into twomain steps growth mediated and product mediated When con-sidering direct biofuel production the main approach is product

mediated for higher lipid hydrogen or ethanol production Whenconsidering biofuel production integrated with other microorgan-isms (Table 5) the main approach is growth mediated for higher

Table 5Integrated biofuel processes working with microalgae

Microalgae System Product Ref

Chlamydomonas reinhardtii (UTEX 90) Enzymatic treatment of algal biomass and conversion to ethanol by Saccharomyces cerevisiae Ethanol [179]Chlamydomonas reinhardtii (UTEX 90) Hydrothermal acid treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [180]Chlorella vulgaris (IAM C-534) Enzymatic treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [181]Synechococcus leopoliensis (IAMM 6) Fermentation of acid treated saccharified algal biomass by yeast Saccharomyces sake (IFO 2347) Ethanol [97]Chlamydomonas reinhardtii Chlorella vulgaris (macroalgae Undaria pinnatifida) Enzymatic treatment of pre-acid hydrolyzed algal biomass fermentation by 4 different strains of Escherichia coli Ethanol [182]Schizocytrium sp Fermentation of hydrothermal treated algal biomass by E coli KO11 Ethanol [183]Microcystis aeruginosa and Anabaena variabilis Hydrolysis and fermentation of Super Critical fluid pretreated algal biomass by Saccharomyces cerevisiae Ethanol [204]Scenedesmus obliquus Fermentation of algal biomass hydrolysate by Kluyveromyces marxianus IGC 2671 Saccharomyces carlsbergensis

ATCC6269 and Saccharomyces bayanusEthanol [205]

Anabaena sp PCC7120 Fermentation of hydrogen produced residual algal biomass by Enterobacter aerogenes Hydrogen [184]Arthrospira (Spirulina) platensis Nannochloropsis sp and Dunaliella tertilecta Anaerobic fermentation of thermal pretreated algal biomass by immobilized Clostridium acetobutylicum Hydrogen acetone

ethanol butanol[206]

Chlorella vulgaris ESP6 Dark fermentation of acid or alkalineenzyme pretreated algal biomass hydrolysate by Clostridium butyricumCGS5

Hydrogen [207]

Chlorella sp Simultaneous hydrolysis and fermentation of algal biomass by sewage sludge consortia Hydrogen [208]Thalassiosira weissflogii Dark fermentation of algal biomass with the thermophilic bacterium Thermotoga neapolitana Hydrogen [209]Chlamydomonas reinhardtii (IAM C-238) Chlorella pyrenoidosa (IAM C-212) andDunaliella tertiolecta (ATCC 30909)

Fermentation of algal biomass by Lactobacillus amylovorous (ATCC 33620) and Rhodobacter sphaeroides RV Hydrogen [185]

Chlamydomonas reinhardtii (IAM C-238) and Dunaliella tertiolecta (ATCC 30909) Fermentation of algal biomass by Lactobacillus amylovorous and Rhodobium marinum (A-501) mixed culture Hydrogen [186]Chlamydomonas (MGA 161) Fermentation of algal biomass by Rhodovulum sulfidophilum (W-1S) Hydrogen [85]Chlamydomonas reinhardtii (C238) Mixed cultivation of Chlamydomonas reinhardtii (C238) with Rhodospirillum rubrum (NCIB 8255) Hydrogen [187]Scnedesmus sp Fermentation of algal biomass by anaerobic digested sludge Hydrogen [188]Arthrospira maxima Anaerobic digestion of algal biomass by sewage sludge consortia Methane [210]Phaeodactylum tricornutum Anaerobic digestion of algal biomass by potato factory origin anaerobic granular sludge Methane [211]Scenedesmus sp Anaerobic digestion of high pressure thermal pretreated raw and residue (from lipid extraction) algal biomass

and by anaerobic digestor sludgeMethane [212]

Scenedesmus sp Anaerobic digestion of ultrasound and thermal pretreated raw algal biomass by sugar factory origin anaerobicgranular sludge

Methane [213]

Scenedesmus sp Anaerobic digestion of mild thermal pretreated raw algal biomass by sugar factory origin anaerobic granularsludge

Methane [214]

Spirulina platensis Anabaena variabilis and Chlorella sp Processing of algal biomass by an integrated system of methanogenic culture and Rhodobacter capsulatus Methane and hydrogen [189]Spirulina platensis (UTEX 1926) Rhodotorula glutinis (2541) Mixed cultivation of microalgae and yeast using waste water Lipid (biodiesel) [190]Spirulina platensis Using excess CO2 from the ethanol fermentation by Saccharomyces cerevisiae Lipid (biodiesel) [119]Botryococcus braunii (two strains BB763 and BB764) Chlorella vulgaris Chlorellapyrenoidosa

Biodiesel production catalyzed by immobilized Penicillium expansum lipase and Candida antarctica lipase B(Novozym 435)

Lipid (biodiesel) [191]

Chlorella vulgaris (21111B) Anaerobic digestion of algal biomass by sewage sludge origin methanogenic culture Methane [112]Chlorella sp and Scenedesmus Anaerobic digestion of algal biomass by sewage sludge culture Methane [106]Chlorella sp Anaerobic digestion of algal biomass by sludge culture Methane [192]Arthrospira platensis Chlamydomonas reinhardtii Chlorella kessleri Dunaliellasalina Euglena gracilis and Scenedesmus obliquus

Anaerobic digestion of algal biomass by sewage sludge culture Methane [107]

Spirulina maxima Anaerobic digestion of algal biomass by sewage sludge culture Methane [193]Chlorella sp and Scenedesmus Anaerobic codigestion of algal biomass with waste paper by methanogenic culture Methane [194]Tetraselmis Anaerobic digestion of algal biomass by methanogenic culture Methane [195]Chlorococcum sp Anaerobic treatment of distillery waste with algal biomass by acidogenicmethanogenic culture Methane [196]Phaeodactylum tricornutum (CCAP10551) Anaerobic digestion of algal biomass by granular seed sludge from digester treating potato processing waste

water dominated by Methanosaeta sp and Methanosarcina spMethane [197]

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 255

biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264256

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

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ndash264258

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 259

technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

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[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

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[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 5: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

Table 3Various studies focusing on lipid productivities as the key element for biodiesel production

Microalgae Effect Time Cultivation PBR type Lightintensity(lE mminus2 sminus1)

Temp(1C)

Medium Maximum production Ref

Botryococcus braunii(UTEX 572)

CO2 14 days Batchndashautotrophic Bubble column 150 2571 Modified Chu 13 5517153 mg Lminus1 dminus1 (21 biomass) with10 CO2 enriched air

2065 mg Lminus1 dminus1 (24) with 55 CO2

containing flue gas

[14]

Botryococcus braunii(765)

CO2 28 days Batchndashautotrophic Airlift (3 L) 150710 25 Modified BG11 1174 mg Lminus1dminus1 (12717083 biomass) with20 CO2 enriched air

[143]

Botryococcus braunii(UTEX 572)

Media components 18 days Batchndashautotrophic Bubble column(06 L)

50 22 Modified BG11 019 g Lminus1 dminus1 (6496 biomass) in lipidoptimized media

018 g Lminus1 dminus1 (5956 biomass) in growthoptimized media

[15]

Botryococcus braunii(KMITL 2)

Light intensity light cycle nitrogenphosphorus iron cultivation time salinity

40 days Batchndashautotrophic Flasks (1 L) 0ndash538(LD cycle)

25 Chlorella 54697313 with 200 mE mminus2 sminus1 continuouslight 222 mg Lminus1 phosphorus and a salinity of0 psu

[144]

Chlamydomonasreinhardtii

pH and CO2 31 days Batchndashautotrophic BIOCOIL (15 L) 220 2571 Artificial or wastewater

05057002 g Lminus1 dminus1 (2525 biomass) with 33CO2 at pH 75

[145]

Chlorella vulgaris(CCAP 211)

Temperature nitrogen concentration andextraction techniques

14 day Batchndashautotrophic Erlenmayer flask(2 L)

70 15ndash25 Guillard F2 20227060 mg Lminus1 dminus1 (14717030) at25 1C

20307040 mg Lminus1 dminus1 (15317051) with0375 g Lminus1 nitrogen concentration

[146]

Chlorella sorokiniana(GXNN01)

Carbon sources and concentrations 70 h Batchndashautotrophicheterotrophic

Erlenmayer flask(015 L)

0ndash80 3072 BBM 028870008 g Lminus1 (028770018 g gDWminus1)with acetate

Glucose concentration of 20 mmol Lminus1 gavethe maximal lipid yield

0048 lipid gminus1DW dayminus1 (232) inmixotrophic perfusion (rate 28 L hminus1)culture

[147]

Chlorella minutisima(UTEX LB-2341)

Long term outdoor production 80 days Batch or perfusionautotrophicndashmixotrophic

Cylindrical vessel(20 L10 200 Ltotal)

0ndash700 30ndash35 Enriched sea water [148]

Chlorellaprotothecoides(UTEX 249)

Carbon source concentration nitrogenconcentration salinity pH level andagitation speed

103 h Batchndashautotrophicmixotrophicheterotrophic

Erlenmeyer flasks(01 L)

8W 26 Modified basal 025 g Lminus1 dminus1 (25257007) with 15 g Lminus1

glucose 69 pH 019 g Lminus1 dminus1 (20337513) with 204 gLminus1

glycerol 71 pH 0177001 g Lminus1 dminus1 (23087318) with

205 g Lminus1 acetate 67 pH

[149]

Chlorellaprotothecoides(SAG 3380)

CO2 14ndash15days

Batchndashautotrophicmixotrophic

Erlenmeyer flasks(025 L)

100710 2471 BG11 with Peptone 213725 DW (Mixotrophic 1 glycerol) 115731 DW (Autotrophic) 358715 DW (Mixotrophic N-deprived)

[150]

Chlorella pyrenoidosa Waste water 10 days BatchndashMixotrophic Flasks (01 L) 63 25ndash27 Diluted piggery wastewater

(with 1000 mg Lminus1 COD) [151]

Chlorella pyrenoidosaFACHB-9

Waste water 120 h Batchfedbatchndashmixotrophic

Flasks (05 L) 405 (1410LD cycle)

2771 Soybean process wastewater

04 g Lminus1 dminus1 (377934 DW) with fed batchculture

[152]

AuxenochlorellaprotothecoidesUMN280

CO2 waste water 12 days Batchndashmixotrophic Roux bottles(058 L)

60 2572 Waste water (05 L)and BG11 seed culture(008 L)

0182 g Lminus1 (1866 DW) without CO2

0418 g Lminus1 (2082 DW) with 1 CO2

0516 gLminus1 (2058 DW) with 5 CO2

[153]

Chlorella vulgaris KNO3 CO2 and light intensity 250 h Batch 24ndash120 25 Artificial sea water [154]

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Table 3 (continued )

Microalgae Effect Time Cultivation PBR type Lightintensity(lE mminus2 sminus1)

Temp(1C)

Medium Maximum production Ref

Membrane spargedcylindrical vessel(5 L)

40 mg Lminus1 dminus1 (20) at 60 mE mminus2sminus1 lightintensity 1 mM KNO3 concentration 1 CO2

enrichmentChlorellavulgarisKCT-CAG10032

CO2 14 days Batchndashautotrophic Bubble column 150 2571 BG11 6917003 mg Lminus1dminus1 (7 biomass) with 10 CO2

enriched air[14]

Chlorella vulgarisBEIJ-H14

Glucose and urea 665 h Fed batchndashheterotrophic

Stirred tank (600 L) Dark 36ndash37 Glucose enrichedmedium

97 dry weight [155]

Chlorella vulgarisCCALA 256

Nutrient limitation 8 days Batchndashautotrophic Thin layer (150 L) 100ndash960 195ndash33

14 SS 032670010 g Lminus1 dminus1 (306705 DW) [156]

Choricystis minor Temperature dilution rate andpostharvest methods

Continuousndashautotrophic

Stirred tank (4 L) 550 10ndash30 BG 11 82 mg Lminus1 dminus1 (213717) at 25 1C and adilution rate of 0014 hminus1

Lipid content increased up to 595716under postharvest conditions withoutphosphate and nitrate

[157]

Nannochloropsisoculata

Temperature nitrogen concentration andextraction techniques

14 days Batchndashautotrophic Erlenmayer Flask(2 L)

70 25ndash38 BBM 9117030 mg Lminus1 dminus1 (14927082) at15 1C

16417011 mg Lminus1 dminus1 (15867059) with0075 gLminus1 nitrogen concentration

[139]

Nannochloropsisoculata

Temperature nitrogen and yeast extractconcentrations

16 days Batchndashphotomixotrophic

Airlift (2 L) 160ndash270 15ndash35 F2 10ndash15 (50 ppm nitrogen) 20-25 (125 ppm nitrogen) 25ndash30 (15 1C) 20ndash25 (35 1C)

[158]

Haematococcuspluvialis

Continuous light intensity or light cyclesno nitrogen or no aeration on production

14 days Batchndashautotrophic Flask 90 24 BBM 15617146 DW Under normal conditions 34857078 DW Under full medium

continuous light with aeration 32997277 DW Under continuous light

aeration no nitrogen

[159]

Neochlorisoleoabundans(UTEX-1185)

Nitrogen sources and concentrations 7 days Batchndashautotrophic Bubble column(1 L)

360 3072 SE 0133 g Lminus1 dminus1 (38) with 5 mM sodium nitrateas nitrogen source

[160]

Neochlorisoleoabundans(UTEX-1185)

Temperature CO2 and nitrate 18 days Batchndashautotrophic Bubble column(1 L)

150 26ndash30 BM 56 biomass with nitrogen starvation at 30 1Ctemperature without CO2 in air

[161]

Neochlorisoleoabundans(UTEX-1185)

Nitrogen starvation 140 h Continuousndashautotrophic

Flat panel airlift(1 L)

270 25 BBM 126 g mminus3 dminus1 (23) continuous culture withno mineral limitation with nitrate starvation

20657013 mg Lminus1dminus1 (9 biomass) with10 CO2 enriched air

3944 mg Lminus1 dminus1 (18) with 55 CO2

containing flue gas 16ndash18 DW with nitrogen deplete two stage

process 10ndash12 DW with single stage process

[162]

Scenedesmus spKCTC AG20831

CO2 14 days Batchndashautotrophic Bubble column 150 2571 BG11 [14]

Tetraselmis suecica Light and nitrogen concentration 9 days Batchndashautotrophic Stirred tank (20 L) 363ndash1331 2071 Modified F2 [163]

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 247

The preferred route for biodiesel production from oils istransesterification rather than pyrolysis and micro-emulsionbecause of the cost and quality concerns [25] Transesterificationis simply the reaction between triacylglycerols and an acyl-acceptor which can be carboxylic acids (acidolysis) alcohols(alcoholysis) or another ester (interesterification) [2526] Biodie-sel production from microalgal oils through transesterificationprocess has several steps (Fig 3)

The reaction can be chemically (acid or base) or biologically(enzyme) catalytic or non-catalytic (high pressure process) [27ndash29]

Homogeneous (NaOH CH3ONa KOH KOCH3) and heterogeneous(alkaline earth metal oxides zeolite KNO3 loaded on Al2O3 KNO3Al2O3 BaO SrO CaO MgO) base catalysts are conventionally used forbiodiesel production They are more effective with an oil having free

Strain selection

- Determination of cell culture condition

- Optimization of lipid production conditions

- Scale -up

Photobioreactor

LightCO2 Nutrients

Separation amp

Refining

Acid Water

CatalystAlcohol Glycerol

Temperature

Fig 3 Microalgal biodiesel productionSource Adapted from Refs [7 4647199200]

fatty acid concentration up to 2 resulting in high reaction rates(4000 faster) and conversion efficiency under lower operationtemperatures compared to acid catalysts But considering watercontent and acidity of the biodiesel feedstock acid catalysts arepreferred to prevent saponification Even if acid catalysts are effectivewith non-edible oils their limitations like the need for higher amountsof alcohol higher temperatures and pressures slower reaction ratesresult in lower yields Both homogeneous and heterogeneous acidcatalysts (sulfuric acid hydrochloric acid phosphoric acid and sulfo-nated organic acids) are used especially in two step biodiesel produc-tion where in the first step the oil reacts with alcohol by acid catalystsand later reacted with the base catalyst This procedure is preferredwith high free fatty acid concentrated oils where the proceduredecreases the value of the free fatty acids to operational levels [1030]

Water

Biomass Harvesting

- Filtration

- Centrifugation

- Sedimentation

- Flotation

Dryer

Oil Extraction

-Chemical

-Biochemical

-Mechanical

Catalyst

-Chemical

-Biological

Oil

Alcohol

Transesterification

Biodiesel

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264248

Conventional technology of chemical catalysis has some con-straints due to the environmental problems related with soapformation and energy demand due to the downstream processesto recover glycerol and catalysts [262831]

Biological catalysis has some advantages over the chemicalcatalysis including lower energy demand moderate reaction con-ditions lower alcohol to oil ratio easier product recovery and highconversion [3132]

Lipases are the key biocatalysts that are used in biodieselproduction Major producer microorganisms for lipases are Aspergil-lus niger Aspergillus oryzae Bacillus pumilis Burkholderla cepaciaCandida antarctica Candida cylindracea Candida lipolytica Candidaparalipolytica Candida rugosa Chromobacterium viscosum Enterobac-ter aerogenes Eremothecium ashbyii Escherichia coli Geotrichumcandidum Mucor miehei Penicillium cyclopium Penicillium expansumPenicillium restrictum Pseudomonas cepacia Pseudomonas fluorescensPseudomonas fragi Rhizopus arrhizus Rhizopus delemar Rhyzomucormiehei Rhizopus oryzae Saccharomyces cerevisiae and Thermomyceslanuginosus which are also commercially important to meet theneeds of the large scale biodiesel processes [3334]

Main bottlenecks of this process include high cost of enzymelow yield due to inactivation longer reaction time slower reactionrate and the amount of water and organic solvents in the reactionmixture [2532]

The limitations in the biocatalysis are managed via the immo-bilization of the lipases in packed bed reactors to prevent washoutand inactivation [35] using whole cell immobilization [26] ionicliquids in enzyme catalysis [3136] genetic modifications andrecombinant microorganisms to enhance the efficiency and theproduction of the enzyme [26] alternative acyl acceptors [37]stepwise processes [3839] moderate polar solvents [40] non-catalytic methods under supercritical conditions [4142] and highpressure processes to stabilize the enzymes [4344]

From the economical point of view which is also importantchemical catalysis is reported to be cheaper than biologicalcatalysis But the modifications like using immobilized biocatalystsand the enhanced reuse can serve a competitive cost compared tothe chemical catalysts [45]

Numerous approaches are still in progress for the optimizationof the biodiesel production process adaptable to different feedtypes compositions and downstream requirements One of thenovel processes mentioned in recent studies is the ldquoMcgyan Processrdquothat consists of a continuous fixed bed reactor that can producebiodiesel using a metal oxide based catalyst The process is analternative method for continuous transesterification and can use awide variety of feedstock does not consume the catalyst reducesthe reaction time from hours to seconds and does not use water ordangerous chemicals [164647] Treatment of the lipids extractedfrom Dunaliella tertiolecta and Nannochloropsis oculata with Mcgyanprocess to produce biodiesel reached up to 85 in the conversion oftriacylglycerides and free fatty acids to alkyl esters [48]

Alternatively by shifting the production route microalgal oilscan be used to produce ldquogreen dieselrdquo by a process known ascatalytic hydroprocessing The basic difference of this with trans-esterification is the usage of hydrogen rather than the alcohol Alsothe by-products like propane water and carbon dioxide differfrom glycerol of transesterification [816] Green diesel has super-iority over biodiesel with its lower oxygen constitution similar tothe petroleum derived fuels with a near zero oxygen content Theprimary goal of the processes is to produce a minimized oxygencontaining green diesel with maximized final energy content[816] Also because of the high paraffinic hydrocarbon contentgreen diesel has higher cetane numbers and energy content onmass basis compared to biodiesel Using the microalgal oils forgreen diesel will be advantageous because of the applicationpotential in the conventional petroleum refinery systems with

existing infrastructure and the by-products (H2O and CO2) can berecycled to be used in the microalgae cultivation again

With the rapid progress in the area of genetic engineering theresearchers can now present the genome sequences of microalgaefor example a lipid producing microalgae specie that has potentialin biofuel production ie Nannochloropsis gaditana genome isnewly finalized and may become a model organism like Chlamy-domonas reinhardtii Chlorella variabilis Micromonas pusila Ostreo-coccus tauri Ostreococcus lucimarinus Thalassiosira psudonanaEmiliana huxleyii Fragilariopsis cylindrus Aerococcus aophageffe-rens Cyanidioschyzon merolae and Phaeodactylum tricornutum withcompleted genomes [4950] By understanding these model micro-organisms in molecular basis we can have the chance to improveproductivities in future applications

The ultimate idea was the excretion of the oils from themicroalgae cells without the need of extraction step This ideawas supported with the studies focusing on Escherichia coli andSaccharomyces cerevisiae to excrete lipids through membraneswith genetic engineering tools [5152]

22 Biohydrogen

Hydrogen with its unique properties is accepted to be arenewable sustainable and environmentally friendly energy car-rier that serve as one of the most promising alternative solution toovercome the growing environmental concerns considering thefuture energy demands [5354]

Today there are various conventional as well as novel strategiesto produce hydrogen from fossil fuels (steam reforming plasmareforming thermal cracking gasification) biomass (pyrolysismicrobial conversion syngas conversion supercritical conversiongasification) and water (photolysis thermolysis electrolysis)incorporating chemical and biological processes [272955] Evenif the hydrogen production is dominated by the chemical pro-cesses using fossil fuels biological processes started to get moreattention since the first studies in the 1920s [56ndash58]

The metabolic routes for biohydrogen production differ accord-ing to the microorganism [2759]

Microalgae

(a) Direct photolysis 2H2O-light-2H2+O2

(b) Indirect photolysis(1) 12H2O+6CO2-light-C6H12O6+6O2

(2) C6H12O6+12H2O-12H2+6CO2Photosynthetic bacteria(a) Photofermentation CH3COOH+2H2O-light-4H2+2CO2

(b) Water-gas shift CO+H2O-H2+CO2Anaerobic bacteria Dark fermentationC6H12O6+2H2O-4H2+2CO2+2CH3COOH

Related with their photosynthetic productivity and light utili-zation efficiency microalgae can perform special biochemical andphotochemical reactions with minimum requirements that makehydrogen production possible under aerobic and anaerobic envir-onments [60ndash62]

Microalga like Anabaena sp [6364] Chlorella pyrenoidosa [65]Chlorella vulgaris [66] Platymonas subcordiformis [6667] Spirulinaplatensis [68] and especially Chlamydomonas reinhardtii [6970] getattention in biohydrogen production

Microalgae use two classes of oxygen sensitive metalloenzymesnitrogenases and hydrogenases that are closely related with thefinal biohydrogen generation process in photosynthesis [6371]

There are several types of hydrogenases like the hup-encodedNiFe-uptake hydrogenases hox-encoded NiFe-bidirectional hydro-genases FeFe hydrogenases NiFeSe-bidirectional hydrogenases

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 249

and Fe-only hydrogenases utilized by bacteria and microalgae Onthe other hand nitrogenases of purple non-sulfur bacteria andheterocyst microalgae can be classified by their metal cofactor asmolybdenum iron and vanadium types [7273]

Nitrogenase is the part of the biological nitrogen fixation andhydrogenase is capable to catalyze hydrogen consuming reactionsBiohydrogen production based on these enzymes differs in energyconsumption Hydrogenase mediated reactions are about threetimes more efficient than nitrogenase catalyzed reactions based onspent energy in the form of ATP On the other hand nitrogenasesare relatively less sensitive to oxygen compared to hydrogenases[74ndash76] Relatively or not because both enzymes are sensitive tooxygen it is important to control culture conditions for optimalhydrogen production

Microalgal biohydrogen production can take place duringphotosynthesis from water by the two photosystems dark fer-mentation of the reduced carbon produced by photosynthesis andphotofermentation by the enzymatic oxidation of intracellularreductants derived from fermentation [77ndash80]

Even if the studies on microalgal biohydrogen started in the 1930s[568182] it was shown that the production can be achieved by theinactivation of photosynthetic water oxidizing activity catalyzed bythe reaction center of photosystem two (PSII) [83ndash85] the productiv-ities could not reach to meaningful levels until there was a novelprotocol depending on sulfur deprivation [69] This protocol dependson the succession of photosynthetic reactions in which oxygenproduction and carbon accumulation take place and anaerobic photo-reactions through which the consumption of stored photosyntheticcellular metabolites for biohydrogen generation take place Sulfurdeprivation triggers the conversion of PSII centers to an intermediatein the PSII repair cycle in other words from a QB-reducing to aQB-nonreducing form resulting in the decrease of photosyntheticoxygen evolution capacity [86ndash88]

Compared to the other methods like using inhibitors (DBMIBDCMU SAL C1-CCP etc) or alternating lightdark cycle the removalof sulfate from the growth medium achieves a reversible inactiva-tion with sustainable and increased hydrogen production [83ndash85]

Most of the recent studies focused on the two stage sulfurdeprivation protocol however as summarized by some of theexample studies from batch to continuous processes with variousprocedures the use of different microalgae is a good sign of theprogress towards the future (Table 4) But again some microalgaelike Platymonas subcordiformis Platymonas helgolandica or Chla-mydomonas moewusii are not sensitive to sulfur deprivation aswell as Chlamydomonas reinhardtii so utilization of inhibitors andnitrogen starvation enhance the hydrogen production [8990]

Also the outdoor studies point out another bottleneck in theproductions Even if the applications in lab scale are givingpromising results outdoor cultures still cannot reach the compar-able levels Microalgae cells have problems to tolerate the lightinhibition and sulfur deprivation when exposed to direct sunlightoutdoors They need to be acclimated to light before the hydrogenproduction phase [91]

Besides the studies on the enhancement of the biohydrogenproduction focusing on culture techniques like utilization of immobi-lized microalgae or stressed cultivations with regard to light andmedium components the progress in genetic engineering to improveproduction levels focuses on engineering truncated antennas of thespecies for better sunlight utilization outdoors without inhibition orengineering oxygen tolerant species that can produce hydrogen inaerobic conditions which is still under investigation [7392]

23 Bioethanol

Bioethanol may be considered as an alternative clean burningfuel because of its environmentally friendly combustion products

with low greenhouse gas effect relative to fossil fuels Todaycommercial bioethanol production is mainly from agriculturalstocks and raw materials like corn rice wheat cassava sugarcane sugar beet and sweet sorghum through biochemical orthermochemical processes [161793] Even though the route ofproduction depends on the raw material it can be summarized asthe breaking of the biomaterial to simple sugars that furtherfermented using alcohol producing microorganisms The producedethanol later separated and concentrated through downstreamprocesses (Fig 4)

Facing the conflict of global energy and food demand therehave been increasing interest and worldwide studies in producingbioethanol from alternative sources like microalgae rather thanfeedstock that has minor impact in the daily life [161793]

Bioethanol from microalgae can be produced through thefermentation of the microalgal biomass or directly through cellularreactions [9495]

When considering ethanol production via fermentation the keyis the accumulation of starch which is a potential substrate thatcan reach half of the microalgas cellular dry biomass Microalgalstarch can be extracted by mechanical or enzymatic means andfurther separated by downstream processes incorporating wateror an organic solvent This starch will be hydrolyzed to glucose tobe used in ethanol fermentation [9697] Production mainly differsfrom other crop raw materials in the first steps of the processbecause microalgae will need special concentration harvestingand mechanical disruption systems related with their cellularphysiology and culturing [98]

Microalgae can also excrete ethanol directly through the cellwalls by means of intracellular processes under dark becauseillumination prevents the formation of ethanol except for minoramounts This process which is reported in some microalgae likeChlorococcum littorale [99] Chlamydomonas reinhardtii [8384]Chlamydomonas moewusii [100] Chlorella vulgaris [101] Oscilla-toria limnetica [102] Oscillatoria limosa [99] Gleocapsa alpicola[103] Spirulina platensis [68] Cyanoteche sp [99] covers theanaerobic metabolism in algae where the assimilation and forma-tion of hydrogen carbon dioxide formate acetate ethanol lactateglycerol and butannediol take place [1783] Degradation of intracel-lular starch which is the main endogenous carbon source storedduring aerobic phototrophic metabolism to pyruvate is accomplishedby the EmbdenndashMeyerhofndashParnas and pentose phosphate pathwaysusing pyruvate decarboxylase and alcohol dehydrogenase enzymes[99102] As stated by Gfeller and Gibbs [83] the lack of ethanolproduction by the microalgae cells during illumination is related withthe absence of available reduced pyridine nucleotides with theassumption of active acetaldehyde and alcohol dehydrogenases Twopossible conversion routes for acetyl-CoA to acetate and ethanol canbe followed In the former route half of the acetyl-CoA is converted toacetate by a deacylase while the rest is reduced to ethanol withacetaldehyde as intermediate In the latter route acetyl-CoA is reducedto acetaldehyde that undergoes a dismutation sequence until theformation of acetate and ethanol [8384]

Enhancing direct microalgal bioethanol production by geneticmanipulations is also under consideration Genes from the ethanolproducing bacterium Zymomonas mobilis was transfered intomicroalgae Synechococcus sp aiming to give the ability to utilizethe fixed carbon for direct ethanol excretion to the culture volumethrough the cell walls [93104]

The novelty of the process lies in the separation of producedbioethanol from the culture medium This process eliminates theharvesting step that decreases the energy costs and water usageassociated with the separation processes required for algae har-vesting and fuel extraction [94105]

Besides bioethanol being the main product the remainingmicroalgal biomass may be used to produce biomethane again

Table 4Microalgal hydrogen production

Microalgae Cultivation Process PBR type Culture medium Hydrogen productionprocedure

Time H2 production Refs

Anabaena variabilis (CCAP 14034B)

Continuousndashphotoautotrophic

Lab Stirred (300 mL) Nitrogen free Allen-Arnon

Nitrogen free Allen-Arnon medium

Under vacuum for 15 min Increased light intensity for

5 h at the 6th day ofcultivation

35 days 12ndash14 mL gminus1DW hminus1 [164]

Anabaena variabilis (ATCC 29413) Continuousndashphotoautotrophic

Lab Vial (14 mL) Allen-Arnon(containing Na2MoO4 orNa3VO4 or neither)

Under argon flushing 80ndash100 h

Up to 5 nmol hminus1 mg Chlaminus1 at pH levels of 7ndash9 with Na3VO4 added cultures

[165]

Anabaena sp PCC 7120 (3hydrogenase mutants from PCC7120)

Batchndashphotoautotrophic Lab Sealed polystyrenecuvettes (1 cm light path47 mL capacity)

BG 11 Nitrogen free BG 11 medium Under anaerobic conditions Various light intensities

32ndash40 h Up to 08ndash1 mmol per cuvette (47 mL) [63]

Anabaena sp PCC 7120 and itsmutant AMC 414

Continuousndashphotoautotrophic

Outdoor Tubular-coiled (435 L) BG 11 Nitrogen free BG 11 medium Under argon atmosphere Nitrogen free BG 11 medium Under anaerobic conditions Increased light intensity

7 days 149 mL hminus1Lminus1PBR (373 mL total) with themutant

[166]

Anabaena variabilis (ATCC 29413) Batchndashphotoautotrophic Lab Panel (500 mL capacity) BG 11 50 h Up to 40ndash50 mL [167]

Chlamydomonas reinhardtii(CC124)

BatchndashphotomixotrophicSynchronous andunsynchronous growth

Lab Stirred glass bottles(12L)

TAP TAP-S medium (transferred bycentrifugation)

140 h 102 mL (with 4 h synchronizedcultures)

86 mL (with unsynchronized cultures)

[168]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotomixotrophic Lab Stirred glass bottles(500 mL)

TAP TAP-S medium transfer bycentrifugation

TAP-S medium inoculationby TAP culture (10inoculation)

175 mL Lminus1 (with centrifuged cultures under20ndash40 mE mminus2sminus1 average light intensity)

[87]

Chlamydomonas reinhardtii(CC124)

Continuousndashphotomixotrophic

Lab Stirred glass bottles(1050 mL)

TAP-S (90 mmol sulfateadded)

TAP-S medium two stagechemostat with aerobicstage and anaerobic stage

TAP-S medium TAP medium with limiting

sulfate (10ndash20 mM) Anaerobic conditions Sulfur free medium Anaerobic

4000 h Up to 058 mL hminus1Lminus1PBR [169]

Chlamydomonas reinhardtii (Dang137C mt+ and a nonmotilemutant CC 1036 pf18 mt+)

Batchndashphotomixotrophic-immobilized

Lab Panel (160 mL) TAP (046 mM sulfatereplete)

23 days 45 mL dayminus1 (380 mL total) [170]

Chlamydomonas reinhardtii (Dang137C mt+)

Batch-photoautotrophicmixotrophic andheterotrophic

Lab Flat glass bottles PBR(15 L volume)

HS (CO2 bubbling) TAPwith or without CO2

bubbling

60ndash80 h 11704 mmol Lminus1 (sim28 mL (hL)minus1) inphotoautotrophic cultures

45716 mmol Lminus1 (sim40 mL (hL)minus1) inphotoheterotrophic cultures

09708 mmol Lminus1 (sim69 mL (hL)minus1)inphotomixotrophic cultures

[171]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotoautotrophic Lab Flat glass bottles PBR(15 L)

High salt HS sulfur free medium Argon purging during the

first 24 h of deprivation TAP-S medium Various dilutions Anaerobic conditions

100 h 7173 mL Lminus1 (175 mE mminus2sminus1 lightintensity pH 77)

5272 mL Lminus1 (420 mE mminus2sminus1 lightintensity pH 74)

[172]

Chlamydomonas reinhardtii(CC124)

Semi continuousndashphotomixotrophic

Lab Stirred tank (25 L) TAP 127 days 1108 mL [173]

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic-immobilized

Lab Vials (75 mL) TAP TA-S-P (no sulfate nophosphate) medium

Alginate entrapped

160ndash180 h

0307002 mol mminus2 (125 mmol mgminus1 Chl hminus1) [174]

Batchndashphotomixotrophic Lab Glass bottles (325 mL) TAP 192 h 395 mmol106 cellsminus1 hminus1 with TAP-S [90]

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ndash264250

harvested cells flushed withor without argon

Anaerobic conditions TAP-S or TAP-N DCMU mixed ethanol

addition Dark anaerobic

fermentation

Chlamydomonas reinhardtii(CC124)

34 mmol106 cellsminus1 hminus1 with TAP-N

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Stirred tank (1 255 L) TAP-S TAP-S medium transfer bycentrifugation

Various mixing time Various light energy Scale-up

192 h Max with 122 kJ sminus1 mminus3 light energy and25 min mixing time

[202]

1 L PBR 1537005 mL Lminus1 hminus1

25 L PBR 1327005 mL Lminus1 hminus1

5 L PBR 1027005 mL Lminus1 hminus1

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Tubular (110 L) TAP-S TAP-S medium transfer bycentrifugation

Modified with silicananoparticle to enhancescattering

48 h 3121571789 mL (06 mL Lminus1 hminus1) [203]

Chlorella pyrenoidosa C-101 Batchndashphotoautotrophic Lab Bubble column (650 mL) Modified Bristol Nitrogen flushing under dark forldquo420rdquo h

60ndash65 h 6910minus2 m3 kgminus1 cell [65]

Chlorella vulgaris MSU 01 Batchndashphotomixotrophic Lab Stirred (500 mL) Modified BG11 and MJ Anaerobic conditions Corn stalk as carbon source

in the medium

6ndash7 days 26 mL [175]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Dark incubation Anaerobic nitrogen

atmosphere Addition of specific effectors

(DCMU DCCD DBMIBand CCCP)

Continuous illuminationafterwards

8 h 0339 mL hminus1 Lminus1 (144 mL) based on1106 cells mLminus1 at 15 μM CCCP addedculture after 8 h of illumination

[66]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Sulfur deprive medium Incubation under dark Anaerobic conditions Continuous illumination

afterwards

50 h 11720 nL hminus1 (with seawater-S medium) [67]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Torus (15 L) Defined mineral Dark incubation Anaerobic nitrogen

atmosphere 15 μM CCCP addition Continuous illumination

afterwards

4ndash6 days 720 mL hminus1 (2366770 mL) [176]

Platymonas helgolandica vartsingtaoensis

Batchndashphotoautotrophic Lab Jars (130 mL) F2 Anaerobic Illuminated -S medium Dark CCCPDCMU or both

added medium

25 h 0002 mmol Lminus1 withndashS medium 0160 mmol Lminus1 with CCCP medium 0014 mmol Lminus1 with DCMU medium 0290 mmol Lminus1 with CCCP

+DCMU medium

[89]

Spirulina platensis (NIES-46) Batchndashphotoautotrophic Lab Erlenmeyer flasks(60 mL)

SOT Nitrogen free medium Under dark

20 h 2 mmol mgDWminus1 [68]

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Table

4(con

tinu

ed)

Micro

alga

eCu

ltivation

Pro

cess

PBRtype

Culture

med

ium

Hyd

roge

npro

duction

pro

cedure

Time

H2pro

duction

Refs

Anae

robicco

nditions

Syne

chocystissp

PCC68

03an

dits

mutantNDH-1

complex

defi

cien

tM55

Batch

ndashphotoa

utotrop

hicndash

encapsu

lated

Lab

Vials

(2mL)

BG

11

Nitroge

natmosphere

Under

cycled

lightan

ddark

exposure

5day

s0005

ndash004

5mM

[177

]

Tetraspo

rasp

CU25

51Batch

ndashphotom

ixotrophic

Lab

Vials

TAP(w

itho

rwithou

t05mM

β-mercaptoethan

olfor

24h)

Su

lfuran

dnitroge

ndep

rive

dmed

ium

Argon

flush

edan

aerobic

atmosphere

424

h173ndash61

7mm

olmgminus

1Chlahminus1

[178

]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264252

through anaerobic digestion for electricity generation The carbondioxide and discharged water formed as by-products of thefermentation can be recycled for the microalgae cultivation tofulfill the biorefinery concept [94105]

24 Biomethane

Today agricultural plants or by-products are conventionalsources for renewable biogas production which is mainly amixture of methane (55ndash75) and carbon dioxide (25ndash45) byanaerobic digestion Biomethane from the biogas can be used as afuel for transportation and electricity generation or for heatingpurposes especially in the rural areas [16106107]

Microalgae with their dominancy over crop plants by means ofproductivity per hectare triggered the attention for the production ofbiogas The solar energy converted and stored by the microalgae cellsthrough photosynthesis can be transformed into energy through theanaerobic digestion to produce methane [106108]

Microalgal biomass having high cellular lipid starch andprotein low cellulose and on the other hand the absence of ligningives a reliable and effective anaerobic digestion These specifica-tions make microalgae a good alternative for effective biomethaneproduction compared to the other crop plants [16107108]

Microalgal biomass can be processed anaerobically step by stepwith specialized groups of bacteria [109]

Hydrolyzation of biopolymers to monosaccharides by hydro-lytic bacteria

Fermentation of the monosaccharides to carboxylic acids andalcohols by fermentative bacteria

Conversion of the acids and alcohols to acetate hydrogen andcarbon dioxide by acetogenic bacteria

Conversion of the end products of acetogenic reactions tomethane and carbon dioxide by methanogenic bacteria

Microalgal biomass remaining after the anaerobic digestion canbe further processed to make fertilizers that can add an extra valueto the overall process Also the carbon dioxide portion of theproduced biogas can be recycled again to cultivate the neededmicroalgal biomass for processing [107110ndash112]

A predicted model of microalgae biomass for digestion toproduce electrical and thermal energy discussed the economicprofitability related with technical aspects of the productionsystem The results showed that the microalgae productivityharvesting concentration and usage of high rate anaerobic diges-ters are the key factors for the economic energy production [113]

A life cycle perspective study using a stochastic model indi-cated that when compared with the conventional crops likeswitch grass canola and corn the environmental impact ofmicroalgal biomass production is higher with respect to energydemand greenhouse gas emissions and water use regardless ofcultivation location Only in overall land use and eutrophicationpotential microalgae present favorable results [114] This mayseem to be a disadvantage to produce biomethane from microalgalbiomass but the studies also supported that the integratedprocesses using proper photobioreactors combining microalgaecultivation and waste water treatment systems for biomethaneproduction will help to reduce the environmental impacts result-ing in a competitive and effective production [11416115]

25 Integrated processes

Relations between parameters and the target products (bio-mass lipid hydrogen ethanol) are important in the selection ofthe microalgae for efficient biofuel production As can be followedfrom the tables summarizing the microalgal biofuel productions

Sugars

- Sugarcane juice

- Molasses

- Sugar beet

Starch

- Corn

- Oats

- Wheat

- Sago Palm

- Cassava

- Banana wastes

- Rye

- Barley

- Triticale

- Sorghum

- Algal biomass

Lignocellulosic materials

- Crop residues

- Cellulose wastes

- Hardwood

- Harbaceous biomass

- Softwood

- Municipal solid wastes

Fermentation

- Saccharomyces cerevisiae

- Schizosaccharomyces pombe

- Zymomonas mobilis

- Saccharomyces bayanus

- Pichia stipitis

- Candida shehatae

- Pachysolen tannophilus

- Mucor indicus

- Chalara parvispora

- T thermosaccharolyticum

- T Ethanolicus

- B Stearothermophilus

- C thermohydrosulfuricum

- C thermocellum

- Milling

- Grinding

- ShredingBreaking hemicellulose

chains

- Physical

- Chemical

- Physicochemical

- Biological

Hydrolization -Detoxification

-Neutralization

Sugars

- Hexoses

- Pentoses

Separation and

Concentration

- Distillation

- Rectification

- Dehydration

ETHANOL

Fig 4 Ethanol production from biomass productionSource Adapted from Refs [9398201]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 253

studies focus on the separation of production processes into twomain steps growth mediated and product mediated When con-sidering direct biofuel production the main approach is product

mediated for higher lipid hydrogen or ethanol production Whenconsidering biofuel production integrated with other microorgan-isms (Table 5) the main approach is growth mediated for higher

Table 5Integrated biofuel processes working with microalgae

Microalgae System Product Ref

Chlamydomonas reinhardtii (UTEX 90) Enzymatic treatment of algal biomass and conversion to ethanol by Saccharomyces cerevisiae Ethanol [179]Chlamydomonas reinhardtii (UTEX 90) Hydrothermal acid treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [180]Chlorella vulgaris (IAM C-534) Enzymatic treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [181]Synechococcus leopoliensis (IAMM 6) Fermentation of acid treated saccharified algal biomass by yeast Saccharomyces sake (IFO 2347) Ethanol [97]Chlamydomonas reinhardtii Chlorella vulgaris (macroalgae Undaria pinnatifida) Enzymatic treatment of pre-acid hydrolyzed algal biomass fermentation by 4 different strains of Escherichia coli Ethanol [182]Schizocytrium sp Fermentation of hydrothermal treated algal biomass by E coli KO11 Ethanol [183]Microcystis aeruginosa and Anabaena variabilis Hydrolysis and fermentation of Super Critical fluid pretreated algal biomass by Saccharomyces cerevisiae Ethanol [204]Scenedesmus obliquus Fermentation of algal biomass hydrolysate by Kluyveromyces marxianus IGC 2671 Saccharomyces carlsbergensis

ATCC6269 and Saccharomyces bayanusEthanol [205]

Anabaena sp PCC7120 Fermentation of hydrogen produced residual algal biomass by Enterobacter aerogenes Hydrogen [184]Arthrospira (Spirulina) platensis Nannochloropsis sp and Dunaliella tertilecta Anaerobic fermentation of thermal pretreated algal biomass by immobilized Clostridium acetobutylicum Hydrogen acetone

ethanol butanol[206]

Chlorella vulgaris ESP6 Dark fermentation of acid or alkalineenzyme pretreated algal biomass hydrolysate by Clostridium butyricumCGS5

Hydrogen [207]

Chlorella sp Simultaneous hydrolysis and fermentation of algal biomass by sewage sludge consortia Hydrogen [208]Thalassiosira weissflogii Dark fermentation of algal biomass with the thermophilic bacterium Thermotoga neapolitana Hydrogen [209]Chlamydomonas reinhardtii (IAM C-238) Chlorella pyrenoidosa (IAM C-212) andDunaliella tertiolecta (ATCC 30909)

Fermentation of algal biomass by Lactobacillus amylovorous (ATCC 33620) and Rhodobacter sphaeroides RV Hydrogen [185]

Chlamydomonas reinhardtii (IAM C-238) and Dunaliella tertiolecta (ATCC 30909) Fermentation of algal biomass by Lactobacillus amylovorous and Rhodobium marinum (A-501) mixed culture Hydrogen [186]Chlamydomonas (MGA 161) Fermentation of algal biomass by Rhodovulum sulfidophilum (W-1S) Hydrogen [85]Chlamydomonas reinhardtii (C238) Mixed cultivation of Chlamydomonas reinhardtii (C238) with Rhodospirillum rubrum (NCIB 8255) Hydrogen [187]Scnedesmus sp Fermentation of algal biomass by anaerobic digested sludge Hydrogen [188]Arthrospira maxima Anaerobic digestion of algal biomass by sewage sludge consortia Methane [210]Phaeodactylum tricornutum Anaerobic digestion of algal biomass by potato factory origin anaerobic granular sludge Methane [211]Scenedesmus sp Anaerobic digestion of high pressure thermal pretreated raw and residue (from lipid extraction) algal biomass

and by anaerobic digestor sludgeMethane [212]

Scenedesmus sp Anaerobic digestion of ultrasound and thermal pretreated raw algal biomass by sugar factory origin anaerobicgranular sludge

Methane [213]

Scenedesmus sp Anaerobic digestion of mild thermal pretreated raw algal biomass by sugar factory origin anaerobic granularsludge

Methane [214]

Spirulina platensis Anabaena variabilis and Chlorella sp Processing of algal biomass by an integrated system of methanogenic culture and Rhodobacter capsulatus Methane and hydrogen [189]Spirulina platensis (UTEX 1926) Rhodotorula glutinis (2541) Mixed cultivation of microalgae and yeast using waste water Lipid (biodiesel) [190]Spirulina platensis Using excess CO2 from the ethanol fermentation by Saccharomyces cerevisiae Lipid (biodiesel) [119]Botryococcus braunii (two strains BB763 and BB764) Chlorella vulgaris Chlorellapyrenoidosa

Biodiesel production catalyzed by immobilized Penicillium expansum lipase and Candida antarctica lipase B(Novozym 435)

Lipid (biodiesel) [191]

Chlorella vulgaris (21111B) Anaerobic digestion of algal biomass by sewage sludge origin methanogenic culture Methane [112]Chlorella sp and Scenedesmus Anaerobic digestion of algal biomass by sewage sludge culture Methane [106]Chlorella sp Anaerobic digestion of algal biomass by sludge culture Methane [192]Arthrospira platensis Chlamydomonas reinhardtii Chlorella kessleri Dunaliellasalina Euglena gracilis and Scenedesmus obliquus

Anaerobic digestion of algal biomass by sewage sludge culture Methane [107]

Spirulina maxima Anaerobic digestion of algal biomass by sewage sludge culture Methane [193]Chlorella sp and Scenedesmus Anaerobic codigestion of algal biomass with waste paper by methanogenic culture Methane [194]Tetraselmis Anaerobic digestion of algal biomass by methanogenic culture Methane [195]Chlorococcum sp Anaerobic treatment of distillery waste with algal biomass by acidogenicmethanogenic culture Methane [196]Phaeodactylum tricornutum (CCAP10551) Anaerobic digestion of algal biomass by granular seed sludge from digester treating potato processing waste

water dominated by Methanosaeta sp and Methanosarcina spMethane [197]

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biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

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technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

[1] EIA (US Energy Information Administration) International Energy Outlook2010 Washington DC 20585 US 2010 langwwweiagovoiafieoindexhtmlrang

[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264262

[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 6: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

Table 3 (continued )

Microalgae Effect Time Cultivation PBR type Lightintensity(lE mminus2 sminus1)

Temp(1C)

Medium Maximum production Ref

Membrane spargedcylindrical vessel(5 L)

40 mg Lminus1 dminus1 (20) at 60 mE mminus2sminus1 lightintensity 1 mM KNO3 concentration 1 CO2

enrichmentChlorellavulgarisKCT-CAG10032

CO2 14 days Batchndashautotrophic Bubble column 150 2571 BG11 6917003 mg Lminus1dminus1 (7 biomass) with 10 CO2

enriched air[14]

Chlorella vulgarisBEIJ-H14

Glucose and urea 665 h Fed batchndashheterotrophic

Stirred tank (600 L) Dark 36ndash37 Glucose enrichedmedium

97 dry weight [155]

Chlorella vulgarisCCALA 256

Nutrient limitation 8 days Batchndashautotrophic Thin layer (150 L) 100ndash960 195ndash33

14 SS 032670010 g Lminus1 dminus1 (306705 DW) [156]

Choricystis minor Temperature dilution rate andpostharvest methods

Continuousndashautotrophic

Stirred tank (4 L) 550 10ndash30 BG 11 82 mg Lminus1 dminus1 (213717) at 25 1C and adilution rate of 0014 hminus1

Lipid content increased up to 595716under postharvest conditions withoutphosphate and nitrate

[157]

Nannochloropsisoculata

Temperature nitrogen concentration andextraction techniques

14 days Batchndashautotrophic Erlenmayer Flask(2 L)

70 25ndash38 BBM 9117030 mg Lminus1 dminus1 (14927082) at15 1C

16417011 mg Lminus1 dminus1 (15867059) with0075 gLminus1 nitrogen concentration

[139]

Nannochloropsisoculata

Temperature nitrogen and yeast extractconcentrations

16 days Batchndashphotomixotrophic

Airlift (2 L) 160ndash270 15ndash35 F2 10ndash15 (50 ppm nitrogen) 20-25 (125 ppm nitrogen) 25ndash30 (15 1C) 20ndash25 (35 1C)

[158]

Haematococcuspluvialis

Continuous light intensity or light cyclesno nitrogen or no aeration on production

14 days Batchndashautotrophic Flask 90 24 BBM 15617146 DW Under normal conditions 34857078 DW Under full medium

continuous light with aeration 32997277 DW Under continuous light

aeration no nitrogen

[159]

Neochlorisoleoabundans(UTEX-1185)

Nitrogen sources and concentrations 7 days Batchndashautotrophic Bubble column(1 L)

360 3072 SE 0133 g Lminus1 dminus1 (38) with 5 mM sodium nitrateas nitrogen source

[160]

Neochlorisoleoabundans(UTEX-1185)

Temperature CO2 and nitrate 18 days Batchndashautotrophic Bubble column(1 L)

150 26ndash30 BM 56 biomass with nitrogen starvation at 30 1Ctemperature without CO2 in air

[161]

Neochlorisoleoabundans(UTEX-1185)

Nitrogen starvation 140 h Continuousndashautotrophic

Flat panel airlift(1 L)

270 25 BBM 126 g mminus3 dminus1 (23) continuous culture withno mineral limitation with nitrate starvation

20657013 mg Lminus1dminus1 (9 biomass) with10 CO2 enriched air

3944 mg Lminus1 dminus1 (18) with 55 CO2

containing flue gas 16ndash18 DW with nitrogen deplete two stage

process 10ndash12 DW with single stage process

[162]

Scenedesmus spKCTC AG20831

CO2 14 days Batchndashautotrophic Bubble column 150 2571 BG11 [14]

Tetraselmis suecica Light and nitrogen concentration 9 days Batchndashautotrophic Stirred tank (20 L) 363ndash1331 2071 Modified F2 [163]

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 247

The preferred route for biodiesel production from oils istransesterification rather than pyrolysis and micro-emulsionbecause of the cost and quality concerns [25] Transesterificationis simply the reaction between triacylglycerols and an acyl-acceptor which can be carboxylic acids (acidolysis) alcohols(alcoholysis) or another ester (interesterification) [2526] Biodie-sel production from microalgal oils through transesterificationprocess has several steps (Fig 3)

The reaction can be chemically (acid or base) or biologically(enzyme) catalytic or non-catalytic (high pressure process) [27ndash29]

Homogeneous (NaOH CH3ONa KOH KOCH3) and heterogeneous(alkaline earth metal oxides zeolite KNO3 loaded on Al2O3 KNO3Al2O3 BaO SrO CaO MgO) base catalysts are conventionally used forbiodiesel production They are more effective with an oil having free

Strain selection

- Determination of cell culture condition

- Optimization of lipid production conditions

- Scale -up

Photobioreactor

LightCO2 Nutrients

Separation amp

Refining

Acid Water

CatalystAlcohol Glycerol

Temperature

Fig 3 Microalgal biodiesel productionSource Adapted from Refs [7 4647199200]

fatty acid concentration up to 2 resulting in high reaction rates(4000 faster) and conversion efficiency under lower operationtemperatures compared to acid catalysts But considering watercontent and acidity of the biodiesel feedstock acid catalysts arepreferred to prevent saponification Even if acid catalysts are effectivewith non-edible oils their limitations like the need for higher amountsof alcohol higher temperatures and pressures slower reaction ratesresult in lower yields Both homogeneous and heterogeneous acidcatalysts (sulfuric acid hydrochloric acid phosphoric acid and sulfo-nated organic acids) are used especially in two step biodiesel produc-tion where in the first step the oil reacts with alcohol by acid catalystsand later reacted with the base catalyst This procedure is preferredwith high free fatty acid concentrated oils where the proceduredecreases the value of the free fatty acids to operational levels [1030]

Water

Biomass Harvesting

- Filtration

- Centrifugation

- Sedimentation

- Flotation

Dryer

Oil Extraction

-Chemical

-Biochemical

-Mechanical

Catalyst

-Chemical

-Biological

Oil

Alcohol

Transesterification

Biodiesel

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264248

Conventional technology of chemical catalysis has some con-straints due to the environmental problems related with soapformation and energy demand due to the downstream processesto recover glycerol and catalysts [262831]

Biological catalysis has some advantages over the chemicalcatalysis including lower energy demand moderate reaction con-ditions lower alcohol to oil ratio easier product recovery and highconversion [3132]

Lipases are the key biocatalysts that are used in biodieselproduction Major producer microorganisms for lipases are Aspergil-lus niger Aspergillus oryzae Bacillus pumilis Burkholderla cepaciaCandida antarctica Candida cylindracea Candida lipolytica Candidaparalipolytica Candida rugosa Chromobacterium viscosum Enterobac-ter aerogenes Eremothecium ashbyii Escherichia coli Geotrichumcandidum Mucor miehei Penicillium cyclopium Penicillium expansumPenicillium restrictum Pseudomonas cepacia Pseudomonas fluorescensPseudomonas fragi Rhizopus arrhizus Rhizopus delemar Rhyzomucormiehei Rhizopus oryzae Saccharomyces cerevisiae and Thermomyceslanuginosus which are also commercially important to meet theneeds of the large scale biodiesel processes [3334]

Main bottlenecks of this process include high cost of enzymelow yield due to inactivation longer reaction time slower reactionrate and the amount of water and organic solvents in the reactionmixture [2532]

The limitations in the biocatalysis are managed via the immo-bilization of the lipases in packed bed reactors to prevent washoutand inactivation [35] using whole cell immobilization [26] ionicliquids in enzyme catalysis [3136] genetic modifications andrecombinant microorganisms to enhance the efficiency and theproduction of the enzyme [26] alternative acyl acceptors [37]stepwise processes [3839] moderate polar solvents [40] non-catalytic methods under supercritical conditions [4142] and highpressure processes to stabilize the enzymes [4344]

From the economical point of view which is also importantchemical catalysis is reported to be cheaper than biologicalcatalysis But the modifications like using immobilized biocatalystsand the enhanced reuse can serve a competitive cost compared tothe chemical catalysts [45]

Numerous approaches are still in progress for the optimizationof the biodiesel production process adaptable to different feedtypes compositions and downstream requirements One of thenovel processes mentioned in recent studies is the ldquoMcgyan Processrdquothat consists of a continuous fixed bed reactor that can producebiodiesel using a metal oxide based catalyst The process is analternative method for continuous transesterification and can use awide variety of feedstock does not consume the catalyst reducesthe reaction time from hours to seconds and does not use water ordangerous chemicals [164647] Treatment of the lipids extractedfrom Dunaliella tertiolecta and Nannochloropsis oculata with Mcgyanprocess to produce biodiesel reached up to 85 in the conversion oftriacylglycerides and free fatty acids to alkyl esters [48]

Alternatively by shifting the production route microalgal oilscan be used to produce ldquogreen dieselrdquo by a process known ascatalytic hydroprocessing The basic difference of this with trans-esterification is the usage of hydrogen rather than the alcohol Alsothe by-products like propane water and carbon dioxide differfrom glycerol of transesterification [816] Green diesel has super-iority over biodiesel with its lower oxygen constitution similar tothe petroleum derived fuels with a near zero oxygen content Theprimary goal of the processes is to produce a minimized oxygencontaining green diesel with maximized final energy content[816] Also because of the high paraffinic hydrocarbon contentgreen diesel has higher cetane numbers and energy content onmass basis compared to biodiesel Using the microalgal oils forgreen diesel will be advantageous because of the applicationpotential in the conventional petroleum refinery systems with

existing infrastructure and the by-products (H2O and CO2) can berecycled to be used in the microalgae cultivation again

With the rapid progress in the area of genetic engineering theresearchers can now present the genome sequences of microalgaefor example a lipid producing microalgae specie that has potentialin biofuel production ie Nannochloropsis gaditana genome isnewly finalized and may become a model organism like Chlamy-domonas reinhardtii Chlorella variabilis Micromonas pusila Ostreo-coccus tauri Ostreococcus lucimarinus Thalassiosira psudonanaEmiliana huxleyii Fragilariopsis cylindrus Aerococcus aophageffe-rens Cyanidioschyzon merolae and Phaeodactylum tricornutum withcompleted genomes [4950] By understanding these model micro-organisms in molecular basis we can have the chance to improveproductivities in future applications

The ultimate idea was the excretion of the oils from themicroalgae cells without the need of extraction step This ideawas supported with the studies focusing on Escherichia coli andSaccharomyces cerevisiae to excrete lipids through membraneswith genetic engineering tools [5152]

22 Biohydrogen

Hydrogen with its unique properties is accepted to be arenewable sustainable and environmentally friendly energy car-rier that serve as one of the most promising alternative solution toovercome the growing environmental concerns considering thefuture energy demands [5354]

Today there are various conventional as well as novel strategiesto produce hydrogen from fossil fuels (steam reforming plasmareforming thermal cracking gasification) biomass (pyrolysismicrobial conversion syngas conversion supercritical conversiongasification) and water (photolysis thermolysis electrolysis)incorporating chemical and biological processes [272955] Evenif the hydrogen production is dominated by the chemical pro-cesses using fossil fuels biological processes started to get moreattention since the first studies in the 1920s [56ndash58]

The metabolic routes for biohydrogen production differ accord-ing to the microorganism [2759]

Microalgae

(a) Direct photolysis 2H2O-light-2H2+O2

(b) Indirect photolysis(1) 12H2O+6CO2-light-C6H12O6+6O2

(2) C6H12O6+12H2O-12H2+6CO2Photosynthetic bacteria(a) Photofermentation CH3COOH+2H2O-light-4H2+2CO2

(b) Water-gas shift CO+H2O-H2+CO2Anaerobic bacteria Dark fermentationC6H12O6+2H2O-4H2+2CO2+2CH3COOH

Related with their photosynthetic productivity and light utili-zation efficiency microalgae can perform special biochemical andphotochemical reactions with minimum requirements that makehydrogen production possible under aerobic and anaerobic envir-onments [60ndash62]

Microalga like Anabaena sp [6364] Chlorella pyrenoidosa [65]Chlorella vulgaris [66] Platymonas subcordiformis [6667] Spirulinaplatensis [68] and especially Chlamydomonas reinhardtii [6970] getattention in biohydrogen production

Microalgae use two classes of oxygen sensitive metalloenzymesnitrogenases and hydrogenases that are closely related with thefinal biohydrogen generation process in photosynthesis [6371]

There are several types of hydrogenases like the hup-encodedNiFe-uptake hydrogenases hox-encoded NiFe-bidirectional hydro-genases FeFe hydrogenases NiFeSe-bidirectional hydrogenases

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 249

and Fe-only hydrogenases utilized by bacteria and microalgae Onthe other hand nitrogenases of purple non-sulfur bacteria andheterocyst microalgae can be classified by their metal cofactor asmolybdenum iron and vanadium types [7273]

Nitrogenase is the part of the biological nitrogen fixation andhydrogenase is capable to catalyze hydrogen consuming reactionsBiohydrogen production based on these enzymes differs in energyconsumption Hydrogenase mediated reactions are about threetimes more efficient than nitrogenase catalyzed reactions based onspent energy in the form of ATP On the other hand nitrogenasesare relatively less sensitive to oxygen compared to hydrogenases[74ndash76] Relatively or not because both enzymes are sensitive tooxygen it is important to control culture conditions for optimalhydrogen production

Microalgal biohydrogen production can take place duringphotosynthesis from water by the two photosystems dark fer-mentation of the reduced carbon produced by photosynthesis andphotofermentation by the enzymatic oxidation of intracellularreductants derived from fermentation [77ndash80]

Even if the studies on microalgal biohydrogen started in the 1930s[568182] it was shown that the production can be achieved by theinactivation of photosynthetic water oxidizing activity catalyzed bythe reaction center of photosystem two (PSII) [83ndash85] the productiv-ities could not reach to meaningful levels until there was a novelprotocol depending on sulfur deprivation [69] This protocol dependson the succession of photosynthetic reactions in which oxygenproduction and carbon accumulation take place and anaerobic photo-reactions through which the consumption of stored photosyntheticcellular metabolites for biohydrogen generation take place Sulfurdeprivation triggers the conversion of PSII centers to an intermediatein the PSII repair cycle in other words from a QB-reducing to aQB-nonreducing form resulting in the decrease of photosyntheticoxygen evolution capacity [86ndash88]

Compared to the other methods like using inhibitors (DBMIBDCMU SAL C1-CCP etc) or alternating lightdark cycle the removalof sulfate from the growth medium achieves a reversible inactiva-tion with sustainable and increased hydrogen production [83ndash85]

Most of the recent studies focused on the two stage sulfurdeprivation protocol however as summarized by some of theexample studies from batch to continuous processes with variousprocedures the use of different microalgae is a good sign of theprogress towards the future (Table 4) But again some microalgaelike Platymonas subcordiformis Platymonas helgolandica or Chla-mydomonas moewusii are not sensitive to sulfur deprivation aswell as Chlamydomonas reinhardtii so utilization of inhibitors andnitrogen starvation enhance the hydrogen production [8990]

Also the outdoor studies point out another bottleneck in theproductions Even if the applications in lab scale are givingpromising results outdoor cultures still cannot reach the compar-able levels Microalgae cells have problems to tolerate the lightinhibition and sulfur deprivation when exposed to direct sunlightoutdoors They need to be acclimated to light before the hydrogenproduction phase [91]

Besides the studies on the enhancement of the biohydrogenproduction focusing on culture techniques like utilization of immobi-lized microalgae or stressed cultivations with regard to light andmedium components the progress in genetic engineering to improveproduction levels focuses on engineering truncated antennas of thespecies for better sunlight utilization outdoors without inhibition orengineering oxygen tolerant species that can produce hydrogen inaerobic conditions which is still under investigation [7392]

23 Bioethanol

Bioethanol may be considered as an alternative clean burningfuel because of its environmentally friendly combustion products

with low greenhouse gas effect relative to fossil fuels Todaycommercial bioethanol production is mainly from agriculturalstocks and raw materials like corn rice wheat cassava sugarcane sugar beet and sweet sorghum through biochemical orthermochemical processes [161793] Even though the route ofproduction depends on the raw material it can be summarized asthe breaking of the biomaterial to simple sugars that furtherfermented using alcohol producing microorganisms The producedethanol later separated and concentrated through downstreamprocesses (Fig 4)

Facing the conflict of global energy and food demand therehave been increasing interest and worldwide studies in producingbioethanol from alternative sources like microalgae rather thanfeedstock that has minor impact in the daily life [161793]

Bioethanol from microalgae can be produced through thefermentation of the microalgal biomass or directly through cellularreactions [9495]

When considering ethanol production via fermentation the keyis the accumulation of starch which is a potential substrate thatcan reach half of the microalgas cellular dry biomass Microalgalstarch can be extracted by mechanical or enzymatic means andfurther separated by downstream processes incorporating wateror an organic solvent This starch will be hydrolyzed to glucose tobe used in ethanol fermentation [9697] Production mainly differsfrom other crop raw materials in the first steps of the processbecause microalgae will need special concentration harvestingand mechanical disruption systems related with their cellularphysiology and culturing [98]

Microalgae can also excrete ethanol directly through the cellwalls by means of intracellular processes under dark becauseillumination prevents the formation of ethanol except for minoramounts This process which is reported in some microalgae likeChlorococcum littorale [99] Chlamydomonas reinhardtii [8384]Chlamydomonas moewusii [100] Chlorella vulgaris [101] Oscilla-toria limnetica [102] Oscillatoria limosa [99] Gleocapsa alpicola[103] Spirulina platensis [68] Cyanoteche sp [99] covers theanaerobic metabolism in algae where the assimilation and forma-tion of hydrogen carbon dioxide formate acetate ethanol lactateglycerol and butannediol take place [1783] Degradation of intracel-lular starch which is the main endogenous carbon source storedduring aerobic phototrophic metabolism to pyruvate is accomplishedby the EmbdenndashMeyerhofndashParnas and pentose phosphate pathwaysusing pyruvate decarboxylase and alcohol dehydrogenase enzymes[99102] As stated by Gfeller and Gibbs [83] the lack of ethanolproduction by the microalgae cells during illumination is related withthe absence of available reduced pyridine nucleotides with theassumption of active acetaldehyde and alcohol dehydrogenases Twopossible conversion routes for acetyl-CoA to acetate and ethanol canbe followed In the former route half of the acetyl-CoA is converted toacetate by a deacylase while the rest is reduced to ethanol withacetaldehyde as intermediate In the latter route acetyl-CoA is reducedto acetaldehyde that undergoes a dismutation sequence until theformation of acetate and ethanol [8384]

Enhancing direct microalgal bioethanol production by geneticmanipulations is also under consideration Genes from the ethanolproducing bacterium Zymomonas mobilis was transfered intomicroalgae Synechococcus sp aiming to give the ability to utilizethe fixed carbon for direct ethanol excretion to the culture volumethrough the cell walls [93104]

The novelty of the process lies in the separation of producedbioethanol from the culture medium This process eliminates theharvesting step that decreases the energy costs and water usageassociated with the separation processes required for algae har-vesting and fuel extraction [94105]

Besides bioethanol being the main product the remainingmicroalgal biomass may be used to produce biomethane again

Table 4Microalgal hydrogen production

Microalgae Cultivation Process PBR type Culture medium Hydrogen productionprocedure

Time H2 production Refs

Anabaena variabilis (CCAP 14034B)

Continuousndashphotoautotrophic

Lab Stirred (300 mL) Nitrogen free Allen-Arnon

Nitrogen free Allen-Arnon medium

Under vacuum for 15 min Increased light intensity for

5 h at the 6th day ofcultivation

35 days 12ndash14 mL gminus1DW hminus1 [164]

Anabaena variabilis (ATCC 29413) Continuousndashphotoautotrophic

Lab Vial (14 mL) Allen-Arnon(containing Na2MoO4 orNa3VO4 or neither)

Under argon flushing 80ndash100 h

Up to 5 nmol hminus1 mg Chlaminus1 at pH levels of 7ndash9 with Na3VO4 added cultures

[165]

Anabaena sp PCC 7120 (3hydrogenase mutants from PCC7120)

Batchndashphotoautotrophic Lab Sealed polystyrenecuvettes (1 cm light path47 mL capacity)

BG 11 Nitrogen free BG 11 medium Under anaerobic conditions Various light intensities

32ndash40 h Up to 08ndash1 mmol per cuvette (47 mL) [63]

Anabaena sp PCC 7120 and itsmutant AMC 414

Continuousndashphotoautotrophic

Outdoor Tubular-coiled (435 L) BG 11 Nitrogen free BG 11 medium Under argon atmosphere Nitrogen free BG 11 medium Under anaerobic conditions Increased light intensity

7 days 149 mL hminus1Lminus1PBR (373 mL total) with themutant

[166]

Anabaena variabilis (ATCC 29413) Batchndashphotoautotrophic Lab Panel (500 mL capacity) BG 11 50 h Up to 40ndash50 mL [167]

Chlamydomonas reinhardtii(CC124)

BatchndashphotomixotrophicSynchronous andunsynchronous growth

Lab Stirred glass bottles(12L)

TAP TAP-S medium (transferred bycentrifugation)

140 h 102 mL (with 4 h synchronizedcultures)

86 mL (with unsynchronized cultures)

[168]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotomixotrophic Lab Stirred glass bottles(500 mL)

TAP TAP-S medium transfer bycentrifugation

TAP-S medium inoculationby TAP culture (10inoculation)

175 mL Lminus1 (with centrifuged cultures under20ndash40 mE mminus2sminus1 average light intensity)

[87]

Chlamydomonas reinhardtii(CC124)

Continuousndashphotomixotrophic

Lab Stirred glass bottles(1050 mL)

TAP-S (90 mmol sulfateadded)

TAP-S medium two stagechemostat with aerobicstage and anaerobic stage

TAP-S medium TAP medium with limiting

sulfate (10ndash20 mM) Anaerobic conditions Sulfur free medium Anaerobic

4000 h Up to 058 mL hminus1Lminus1PBR [169]

Chlamydomonas reinhardtii (Dang137C mt+ and a nonmotilemutant CC 1036 pf18 mt+)

Batchndashphotomixotrophic-immobilized

Lab Panel (160 mL) TAP (046 mM sulfatereplete)

23 days 45 mL dayminus1 (380 mL total) [170]

Chlamydomonas reinhardtii (Dang137C mt+)

Batch-photoautotrophicmixotrophic andheterotrophic

Lab Flat glass bottles PBR(15 L volume)

HS (CO2 bubbling) TAPwith or without CO2

bubbling

60ndash80 h 11704 mmol Lminus1 (sim28 mL (hL)minus1) inphotoautotrophic cultures

45716 mmol Lminus1 (sim40 mL (hL)minus1) inphotoheterotrophic cultures

09708 mmol Lminus1 (sim69 mL (hL)minus1)inphotomixotrophic cultures

[171]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotoautotrophic Lab Flat glass bottles PBR(15 L)

High salt HS sulfur free medium Argon purging during the

first 24 h of deprivation TAP-S medium Various dilutions Anaerobic conditions

100 h 7173 mL Lminus1 (175 mE mminus2sminus1 lightintensity pH 77)

5272 mL Lminus1 (420 mE mminus2sminus1 lightintensity pH 74)

[172]

Chlamydomonas reinhardtii(CC124)

Semi continuousndashphotomixotrophic

Lab Stirred tank (25 L) TAP 127 days 1108 mL [173]

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic-immobilized

Lab Vials (75 mL) TAP TA-S-P (no sulfate nophosphate) medium

Alginate entrapped

160ndash180 h

0307002 mol mminus2 (125 mmol mgminus1 Chl hminus1) [174]

Batchndashphotomixotrophic Lab Glass bottles (325 mL) TAP 192 h 395 mmol106 cellsminus1 hminus1 with TAP-S [90]

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harvested cells flushed withor without argon

Anaerobic conditions TAP-S or TAP-N DCMU mixed ethanol

addition Dark anaerobic

fermentation

Chlamydomonas reinhardtii(CC124)

34 mmol106 cellsminus1 hminus1 with TAP-N

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Stirred tank (1 255 L) TAP-S TAP-S medium transfer bycentrifugation

Various mixing time Various light energy Scale-up

192 h Max with 122 kJ sminus1 mminus3 light energy and25 min mixing time

[202]

1 L PBR 1537005 mL Lminus1 hminus1

25 L PBR 1327005 mL Lminus1 hminus1

5 L PBR 1027005 mL Lminus1 hminus1

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Tubular (110 L) TAP-S TAP-S medium transfer bycentrifugation

Modified with silicananoparticle to enhancescattering

48 h 3121571789 mL (06 mL Lminus1 hminus1) [203]

Chlorella pyrenoidosa C-101 Batchndashphotoautotrophic Lab Bubble column (650 mL) Modified Bristol Nitrogen flushing under dark forldquo420rdquo h

60ndash65 h 6910minus2 m3 kgminus1 cell [65]

Chlorella vulgaris MSU 01 Batchndashphotomixotrophic Lab Stirred (500 mL) Modified BG11 and MJ Anaerobic conditions Corn stalk as carbon source

in the medium

6ndash7 days 26 mL [175]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Dark incubation Anaerobic nitrogen

atmosphere Addition of specific effectors

(DCMU DCCD DBMIBand CCCP)

Continuous illuminationafterwards

8 h 0339 mL hminus1 Lminus1 (144 mL) based on1106 cells mLminus1 at 15 μM CCCP addedculture after 8 h of illumination

[66]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Sulfur deprive medium Incubation under dark Anaerobic conditions Continuous illumination

afterwards

50 h 11720 nL hminus1 (with seawater-S medium) [67]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Torus (15 L) Defined mineral Dark incubation Anaerobic nitrogen

atmosphere 15 μM CCCP addition Continuous illumination

afterwards

4ndash6 days 720 mL hminus1 (2366770 mL) [176]

Platymonas helgolandica vartsingtaoensis

Batchndashphotoautotrophic Lab Jars (130 mL) F2 Anaerobic Illuminated -S medium Dark CCCPDCMU or both

added medium

25 h 0002 mmol Lminus1 withndashS medium 0160 mmol Lminus1 with CCCP medium 0014 mmol Lminus1 with DCMU medium 0290 mmol Lminus1 with CCCP

+DCMU medium

[89]

Spirulina platensis (NIES-46) Batchndashphotoautotrophic Lab Erlenmeyer flasks(60 mL)

SOT Nitrogen free medium Under dark

20 h 2 mmol mgDWminus1 [68]

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Table

4(con

tinu

ed)

Micro

alga

eCu

ltivation

Pro

cess

PBRtype

Culture

med

ium

Hyd

roge

npro

duction

pro

cedure

Time

H2pro

duction

Refs

Anae

robicco

nditions

Syne

chocystissp

PCC68

03an

dits

mutantNDH-1

complex

defi

cien

tM55

Batch

ndashphotoa

utotrop

hicndash

encapsu

lated

Lab

Vials

(2mL)

BG

11

Nitroge

natmosphere

Under

cycled

lightan

ddark

exposure

5day

s0005

ndash004

5mM

[177

]

Tetraspo

rasp

CU25

51Batch

ndashphotom

ixotrophic

Lab

Vials

TAP(w

itho

rwithou

t05mM

β-mercaptoethan

olfor

24h)

Su

lfuran

dnitroge

ndep

rive

dmed

ium

Argon

flush

edan

aerobic

atmosphere

424

h173ndash61

7mm

olmgminus

1Chlahminus1

[178

]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264252

through anaerobic digestion for electricity generation The carbondioxide and discharged water formed as by-products of thefermentation can be recycled for the microalgae cultivation tofulfill the biorefinery concept [94105]

24 Biomethane

Today agricultural plants or by-products are conventionalsources for renewable biogas production which is mainly amixture of methane (55ndash75) and carbon dioxide (25ndash45) byanaerobic digestion Biomethane from the biogas can be used as afuel for transportation and electricity generation or for heatingpurposes especially in the rural areas [16106107]

Microalgae with their dominancy over crop plants by means ofproductivity per hectare triggered the attention for the production ofbiogas The solar energy converted and stored by the microalgae cellsthrough photosynthesis can be transformed into energy through theanaerobic digestion to produce methane [106108]

Microalgal biomass having high cellular lipid starch andprotein low cellulose and on the other hand the absence of ligningives a reliable and effective anaerobic digestion These specifica-tions make microalgae a good alternative for effective biomethaneproduction compared to the other crop plants [16107108]

Microalgal biomass can be processed anaerobically step by stepwith specialized groups of bacteria [109]

Hydrolyzation of biopolymers to monosaccharides by hydro-lytic bacteria

Fermentation of the monosaccharides to carboxylic acids andalcohols by fermentative bacteria

Conversion of the acids and alcohols to acetate hydrogen andcarbon dioxide by acetogenic bacteria

Conversion of the end products of acetogenic reactions tomethane and carbon dioxide by methanogenic bacteria

Microalgal biomass remaining after the anaerobic digestion canbe further processed to make fertilizers that can add an extra valueto the overall process Also the carbon dioxide portion of theproduced biogas can be recycled again to cultivate the neededmicroalgal biomass for processing [107110ndash112]

A predicted model of microalgae biomass for digestion toproduce electrical and thermal energy discussed the economicprofitability related with technical aspects of the productionsystem The results showed that the microalgae productivityharvesting concentration and usage of high rate anaerobic diges-ters are the key factors for the economic energy production [113]

A life cycle perspective study using a stochastic model indi-cated that when compared with the conventional crops likeswitch grass canola and corn the environmental impact ofmicroalgal biomass production is higher with respect to energydemand greenhouse gas emissions and water use regardless ofcultivation location Only in overall land use and eutrophicationpotential microalgae present favorable results [114] This mayseem to be a disadvantage to produce biomethane from microalgalbiomass but the studies also supported that the integratedprocesses using proper photobioreactors combining microalgaecultivation and waste water treatment systems for biomethaneproduction will help to reduce the environmental impacts result-ing in a competitive and effective production [11416115]

25 Integrated processes

Relations between parameters and the target products (bio-mass lipid hydrogen ethanol) are important in the selection ofthe microalgae for efficient biofuel production As can be followedfrom the tables summarizing the microalgal biofuel productions

Sugars

- Sugarcane juice

- Molasses

- Sugar beet

Starch

- Corn

- Oats

- Wheat

- Sago Palm

- Cassava

- Banana wastes

- Rye

- Barley

- Triticale

- Sorghum

- Algal biomass

Lignocellulosic materials

- Crop residues

- Cellulose wastes

- Hardwood

- Harbaceous biomass

- Softwood

- Municipal solid wastes

Fermentation

- Saccharomyces cerevisiae

- Schizosaccharomyces pombe

- Zymomonas mobilis

- Saccharomyces bayanus

- Pichia stipitis

- Candida shehatae

- Pachysolen tannophilus

- Mucor indicus

- Chalara parvispora

- T thermosaccharolyticum

- T Ethanolicus

- B Stearothermophilus

- C thermohydrosulfuricum

- C thermocellum

- Milling

- Grinding

- ShredingBreaking hemicellulose

chains

- Physical

- Chemical

- Physicochemical

- Biological

Hydrolization -Detoxification

-Neutralization

Sugars

- Hexoses

- Pentoses

Separation and

Concentration

- Distillation

- Rectification

- Dehydration

ETHANOL

Fig 4 Ethanol production from biomass productionSource Adapted from Refs [9398201]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 253

studies focus on the separation of production processes into twomain steps growth mediated and product mediated When con-sidering direct biofuel production the main approach is product

mediated for higher lipid hydrogen or ethanol production Whenconsidering biofuel production integrated with other microorgan-isms (Table 5) the main approach is growth mediated for higher

Table 5Integrated biofuel processes working with microalgae

Microalgae System Product Ref

Chlamydomonas reinhardtii (UTEX 90) Enzymatic treatment of algal biomass and conversion to ethanol by Saccharomyces cerevisiae Ethanol [179]Chlamydomonas reinhardtii (UTEX 90) Hydrothermal acid treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [180]Chlorella vulgaris (IAM C-534) Enzymatic treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [181]Synechococcus leopoliensis (IAMM 6) Fermentation of acid treated saccharified algal biomass by yeast Saccharomyces sake (IFO 2347) Ethanol [97]Chlamydomonas reinhardtii Chlorella vulgaris (macroalgae Undaria pinnatifida) Enzymatic treatment of pre-acid hydrolyzed algal biomass fermentation by 4 different strains of Escherichia coli Ethanol [182]Schizocytrium sp Fermentation of hydrothermal treated algal biomass by E coli KO11 Ethanol [183]Microcystis aeruginosa and Anabaena variabilis Hydrolysis and fermentation of Super Critical fluid pretreated algal biomass by Saccharomyces cerevisiae Ethanol [204]Scenedesmus obliquus Fermentation of algal biomass hydrolysate by Kluyveromyces marxianus IGC 2671 Saccharomyces carlsbergensis

ATCC6269 and Saccharomyces bayanusEthanol [205]

Anabaena sp PCC7120 Fermentation of hydrogen produced residual algal biomass by Enterobacter aerogenes Hydrogen [184]Arthrospira (Spirulina) platensis Nannochloropsis sp and Dunaliella tertilecta Anaerobic fermentation of thermal pretreated algal biomass by immobilized Clostridium acetobutylicum Hydrogen acetone

ethanol butanol[206]

Chlorella vulgaris ESP6 Dark fermentation of acid or alkalineenzyme pretreated algal biomass hydrolysate by Clostridium butyricumCGS5

Hydrogen [207]

Chlorella sp Simultaneous hydrolysis and fermentation of algal biomass by sewage sludge consortia Hydrogen [208]Thalassiosira weissflogii Dark fermentation of algal biomass with the thermophilic bacterium Thermotoga neapolitana Hydrogen [209]Chlamydomonas reinhardtii (IAM C-238) Chlorella pyrenoidosa (IAM C-212) andDunaliella tertiolecta (ATCC 30909)

Fermentation of algal biomass by Lactobacillus amylovorous (ATCC 33620) and Rhodobacter sphaeroides RV Hydrogen [185]

Chlamydomonas reinhardtii (IAM C-238) and Dunaliella tertiolecta (ATCC 30909) Fermentation of algal biomass by Lactobacillus amylovorous and Rhodobium marinum (A-501) mixed culture Hydrogen [186]Chlamydomonas (MGA 161) Fermentation of algal biomass by Rhodovulum sulfidophilum (W-1S) Hydrogen [85]Chlamydomonas reinhardtii (C238) Mixed cultivation of Chlamydomonas reinhardtii (C238) with Rhodospirillum rubrum (NCIB 8255) Hydrogen [187]Scnedesmus sp Fermentation of algal biomass by anaerobic digested sludge Hydrogen [188]Arthrospira maxima Anaerobic digestion of algal biomass by sewage sludge consortia Methane [210]Phaeodactylum tricornutum Anaerobic digestion of algal biomass by potato factory origin anaerobic granular sludge Methane [211]Scenedesmus sp Anaerobic digestion of high pressure thermal pretreated raw and residue (from lipid extraction) algal biomass

and by anaerobic digestor sludgeMethane [212]

Scenedesmus sp Anaerobic digestion of ultrasound and thermal pretreated raw algal biomass by sugar factory origin anaerobicgranular sludge

Methane [213]

Scenedesmus sp Anaerobic digestion of mild thermal pretreated raw algal biomass by sugar factory origin anaerobic granularsludge

Methane [214]

Spirulina platensis Anabaena variabilis and Chlorella sp Processing of algal biomass by an integrated system of methanogenic culture and Rhodobacter capsulatus Methane and hydrogen [189]Spirulina platensis (UTEX 1926) Rhodotorula glutinis (2541) Mixed cultivation of microalgae and yeast using waste water Lipid (biodiesel) [190]Spirulina platensis Using excess CO2 from the ethanol fermentation by Saccharomyces cerevisiae Lipid (biodiesel) [119]Botryococcus braunii (two strains BB763 and BB764) Chlorella vulgaris Chlorellapyrenoidosa

Biodiesel production catalyzed by immobilized Penicillium expansum lipase and Candida antarctica lipase B(Novozym 435)

Lipid (biodiesel) [191]

Chlorella vulgaris (21111B) Anaerobic digestion of algal biomass by sewage sludge origin methanogenic culture Methane [112]Chlorella sp and Scenedesmus Anaerobic digestion of algal biomass by sewage sludge culture Methane [106]Chlorella sp Anaerobic digestion of algal biomass by sludge culture Methane [192]Arthrospira platensis Chlamydomonas reinhardtii Chlorella kessleri Dunaliellasalina Euglena gracilis and Scenedesmus obliquus

Anaerobic digestion of algal biomass by sewage sludge culture Methane [107]

Spirulina maxima Anaerobic digestion of algal biomass by sewage sludge culture Methane [193]Chlorella sp and Scenedesmus Anaerobic codigestion of algal biomass with waste paper by methanogenic culture Methane [194]Tetraselmis Anaerobic digestion of algal biomass by methanogenic culture Methane [195]Chlorococcum sp Anaerobic treatment of distillery waste with algal biomass by acidogenicmethanogenic culture Methane [196]Phaeodactylum tricornutum (CCAP10551) Anaerobic digestion of algal biomass by granular seed sludge from digester treating potato processing waste

water dominated by Methanosaeta sp and Methanosarcina spMethane [197]

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 255

biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264256

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

SSOncel

Renew

ableand

SustainableEnergy

Review

s26

(2013)241

ndash264258

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 259

technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

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[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

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[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 7: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 247

The preferred route for biodiesel production from oils istransesterification rather than pyrolysis and micro-emulsionbecause of the cost and quality concerns [25] Transesterificationis simply the reaction between triacylglycerols and an acyl-acceptor which can be carboxylic acids (acidolysis) alcohols(alcoholysis) or another ester (interesterification) [2526] Biodie-sel production from microalgal oils through transesterificationprocess has several steps (Fig 3)

The reaction can be chemically (acid or base) or biologically(enzyme) catalytic or non-catalytic (high pressure process) [27ndash29]

Homogeneous (NaOH CH3ONa KOH KOCH3) and heterogeneous(alkaline earth metal oxides zeolite KNO3 loaded on Al2O3 KNO3Al2O3 BaO SrO CaO MgO) base catalysts are conventionally used forbiodiesel production They are more effective with an oil having free

Strain selection

- Determination of cell culture condition

- Optimization of lipid production conditions

- Scale -up

Photobioreactor

LightCO2 Nutrients

Separation amp

Refining

Acid Water

CatalystAlcohol Glycerol

Temperature

Fig 3 Microalgal biodiesel productionSource Adapted from Refs [7 4647199200]

fatty acid concentration up to 2 resulting in high reaction rates(4000 faster) and conversion efficiency under lower operationtemperatures compared to acid catalysts But considering watercontent and acidity of the biodiesel feedstock acid catalysts arepreferred to prevent saponification Even if acid catalysts are effectivewith non-edible oils their limitations like the need for higher amountsof alcohol higher temperatures and pressures slower reaction ratesresult in lower yields Both homogeneous and heterogeneous acidcatalysts (sulfuric acid hydrochloric acid phosphoric acid and sulfo-nated organic acids) are used especially in two step biodiesel produc-tion where in the first step the oil reacts with alcohol by acid catalystsand later reacted with the base catalyst This procedure is preferredwith high free fatty acid concentrated oils where the proceduredecreases the value of the free fatty acids to operational levels [1030]

Water

Biomass Harvesting

- Filtration

- Centrifugation

- Sedimentation

- Flotation

Dryer

Oil Extraction

-Chemical

-Biochemical

-Mechanical

Catalyst

-Chemical

-Biological

Oil

Alcohol

Transesterification

Biodiesel

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264248

Conventional technology of chemical catalysis has some con-straints due to the environmental problems related with soapformation and energy demand due to the downstream processesto recover glycerol and catalysts [262831]

Biological catalysis has some advantages over the chemicalcatalysis including lower energy demand moderate reaction con-ditions lower alcohol to oil ratio easier product recovery and highconversion [3132]

Lipases are the key biocatalysts that are used in biodieselproduction Major producer microorganisms for lipases are Aspergil-lus niger Aspergillus oryzae Bacillus pumilis Burkholderla cepaciaCandida antarctica Candida cylindracea Candida lipolytica Candidaparalipolytica Candida rugosa Chromobacterium viscosum Enterobac-ter aerogenes Eremothecium ashbyii Escherichia coli Geotrichumcandidum Mucor miehei Penicillium cyclopium Penicillium expansumPenicillium restrictum Pseudomonas cepacia Pseudomonas fluorescensPseudomonas fragi Rhizopus arrhizus Rhizopus delemar Rhyzomucormiehei Rhizopus oryzae Saccharomyces cerevisiae and Thermomyceslanuginosus which are also commercially important to meet theneeds of the large scale biodiesel processes [3334]

Main bottlenecks of this process include high cost of enzymelow yield due to inactivation longer reaction time slower reactionrate and the amount of water and organic solvents in the reactionmixture [2532]

The limitations in the biocatalysis are managed via the immo-bilization of the lipases in packed bed reactors to prevent washoutand inactivation [35] using whole cell immobilization [26] ionicliquids in enzyme catalysis [3136] genetic modifications andrecombinant microorganisms to enhance the efficiency and theproduction of the enzyme [26] alternative acyl acceptors [37]stepwise processes [3839] moderate polar solvents [40] non-catalytic methods under supercritical conditions [4142] and highpressure processes to stabilize the enzymes [4344]

From the economical point of view which is also importantchemical catalysis is reported to be cheaper than biologicalcatalysis But the modifications like using immobilized biocatalystsand the enhanced reuse can serve a competitive cost compared tothe chemical catalysts [45]

Numerous approaches are still in progress for the optimizationof the biodiesel production process adaptable to different feedtypes compositions and downstream requirements One of thenovel processes mentioned in recent studies is the ldquoMcgyan Processrdquothat consists of a continuous fixed bed reactor that can producebiodiesel using a metal oxide based catalyst The process is analternative method for continuous transesterification and can use awide variety of feedstock does not consume the catalyst reducesthe reaction time from hours to seconds and does not use water ordangerous chemicals [164647] Treatment of the lipids extractedfrom Dunaliella tertiolecta and Nannochloropsis oculata with Mcgyanprocess to produce biodiesel reached up to 85 in the conversion oftriacylglycerides and free fatty acids to alkyl esters [48]

Alternatively by shifting the production route microalgal oilscan be used to produce ldquogreen dieselrdquo by a process known ascatalytic hydroprocessing The basic difference of this with trans-esterification is the usage of hydrogen rather than the alcohol Alsothe by-products like propane water and carbon dioxide differfrom glycerol of transesterification [816] Green diesel has super-iority over biodiesel with its lower oxygen constitution similar tothe petroleum derived fuels with a near zero oxygen content Theprimary goal of the processes is to produce a minimized oxygencontaining green diesel with maximized final energy content[816] Also because of the high paraffinic hydrocarbon contentgreen diesel has higher cetane numbers and energy content onmass basis compared to biodiesel Using the microalgal oils forgreen diesel will be advantageous because of the applicationpotential in the conventional petroleum refinery systems with

existing infrastructure and the by-products (H2O and CO2) can berecycled to be used in the microalgae cultivation again

With the rapid progress in the area of genetic engineering theresearchers can now present the genome sequences of microalgaefor example a lipid producing microalgae specie that has potentialin biofuel production ie Nannochloropsis gaditana genome isnewly finalized and may become a model organism like Chlamy-domonas reinhardtii Chlorella variabilis Micromonas pusila Ostreo-coccus tauri Ostreococcus lucimarinus Thalassiosira psudonanaEmiliana huxleyii Fragilariopsis cylindrus Aerococcus aophageffe-rens Cyanidioschyzon merolae and Phaeodactylum tricornutum withcompleted genomes [4950] By understanding these model micro-organisms in molecular basis we can have the chance to improveproductivities in future applications

The ultimate idea was the excretion of the oils from themicroalgae cells without the need of extraction step This ideawas supported with the studies focusing on Escherichia coli andSaccharomyces cerevisiae to excrete lipids through membraneswith genetic engineering tools [5152]

22 Biohydrogen

Hydrogen with its unique properties is accepted to be arenewable sustainable and environmentally friendly energy car-rier that serve as one of the most promising alternative solution toovercome the growing environmental concerns considering thefuture energy demands [5354]

Today there are various conventional as well as novel strategiesto produce hydrogen from fossil fuels (steam reforming plasmareforming thermal cracking gasification) biomass (pyrolysismicrobial conversion syngas conversion supercritical conversiongasification) and water (photolysis thermolysis electrolysis)incorporating chemical and biological processes [272955] Evenif the hydrogen production is dominated by the chemical pro-cesses using fossil fuels biological processes started to get moreattention since the first studies in the 1920s [56ndash58]

The metabolic routes for biohydrogen production differ accord-ing to the microorganism [2759]

Microalgae

(a) Direct photolysis 2H2O-light-2H2+O2

(b) Indirect photolysis(1) 12H2O+6CO2-light-C6H12O6+6O2

(2) C6H12O6+12H2O-12H2+6CO2Photosynthetic bacteria(a) Photofermentation CH3COOH+2H2O-light-4H2+2CO2

(b) Water-gas shift CO+H2O-H2+CO2Anaerobic bacteria Dark fermentationC6H12O6+2H2O-4H2+2CO2+2CH3COOH

Related with their photosynthetic productivity and light utili-zation efficiency microalgae can perform special biochemical andphotochemical reactions with minimum requirements that makehydrogen production possible under aerobic and anaerobic envir-onments [60ndash62]

Microalga like Anabaena sp [6364] Chlorella pyrenoidosa [65]Chlorella vulgaris [66] Platymonas subcordiformis [6667] Spirulinaplatensis [68] and especially Chlamydomonas reinhardtii [6970] getattention in biohydrogen production

Microalgae use two classes of oxygen sensitive metalloenzymesnitrogenases and hydrogenases that are closely related with thefinal biohydrogen generation process in photosynthesis [6371]

There are several types of hydrogenases like the hup-encodedNiFe-uptake hydrogenases hox-encoded NiFe-bidirectional hydro-genases FeFe hydrogenases NiFeSe-bidirectional hydrogenases

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 249

and Fe-only hydrogenases utilized by bacteria and microalgae Onthe other hand nitrogenases of purple non-sulfur bacteria andheterocyst microalgae can be classified by their metal cofactor asmolybdenum iron and vanadium types [7273]

Nitrogenase is the part of the biological nitrogen fixation andhydrogenase is capable to catalyze hydrogen consuming reactionsBiohydrogen production based on these enzymes differs in energyconsumption Hydrogenase mediated reactions are about threetimes more efficient than nitrogenase catalyzed reactions based onspent energy in the form of ATP On the other hand nitrogenasesare relatively less sensitive to oxygen compared to hydrogenases[74ndash76] Relatively or not because both enzymes are sensitive tooxygen it is important to control culture conditions for optimalhydrogen production

Microalgal biohydrogen production can take place duringphotosynthesis from water by the two photosystems dark fer-mentation of the reduced carbon produced by photosynthesis andphotofermentation by the enzymatic oxidation of intracellularreductants derived from fermentation [77ndash80]

Even if the studies on microalgal biohydrogen started in the 1930s[568182] it was shown that the production can be achieved by theinactivation of photosynthetic water oxidizing activity catalyzed bythe reaction center of photosystem two (PSII) [83ndash85] the productiv-ities could not reach to meaningful levels until there was a novelprotocol depending on sulfur deprivation [69] This protocol dependson the succession of photosynthetic reactions in which oxygenproduction and carbon accumulation take place and anaerobic photo-reactions through which the consumption of stored photosyntheticcellular metabolites for biohydrogen generation take place Sulfurdeprivation triggers the conversion of PSII centers to an intermediatein the PSII repair cycle in other words from a QB-reducing to aQB-nonreducing form resulting in the decrease of photosyntheticoxygen evolution capacity [86ndash88]

Compared to the other methods like using inhibitors (DBMIBDCMU SAL C1-CCP etc) or alternating lightdark cycle the removalof sulfate from the growth medium achieves a reversible inactiva-tion with sustainable and increased hydrogen production [83ndash85]

Most of the recent studies focused on the two stage sulfurdeprivation protocol however as summarized by some of theexample studies from batch to continuous processes with variousprocedures the use of different microalgae is a good sign of theprogress towards the future (Table 4) But again some microalgaelike Platymonas subcordiformis Platymonas helgolandica or Chla-mydomonas moewusii are not sensitive to sulfur deprivation aswell as Chlamydomonas reinhardtii so utilization of inhibitors andnitrogen starvation enhance the hydrogen production [8990]

Also the outdoor studies point out another bottleneck in theproductions Even if the applications in lab scale are givingpromising results outdoor cultures still cannot reach the compar-able levels Microalgae cells have problems to tolerate the lightinhibition and sulfur deprivation when exposed to direct sunlightoutdoors They need to be acclimated to light before the hydrogenproduction phase [91]

Besides the studies on the enhancement of the biohydrogenproduction focusing on culture techniques like utilization of immobi-lized microalgae or stressed cultivations with regard to light andmedium components the progress in genetic engineering to improveproduction levels focuses on engineering truncated antennas of thespecies for better sunlight utilization outdoors without inhibition orengineering oxygen tolerant species that can produce hydrogen inaerobic conditions which is still under investigation [7392]

23 Bioethanol

Bioethanol may be considered as an alternative clean burningfuel because of its environmentally friendly combustion products

with low greenhouse gas effect relative to fossil fuels Todaycommercial bioethanol production is mainly from agriculturalstocks and raw materials like corn rice wheat cassava sugarcane sugar beet and sweet sorghum through biochemical orthermochemical processes [161793] Even though the route ofproduction depends on the raw material it can be summarized asthe breaking of the biomaterial to simple sugars that furtherfermented using alcohol producing microorganisms The producedethanol later separated and concentrated through downstreamprocesses (Fig 4)

Facing the conflict of global energy and food demand therehave been increasing interest and worldwide studies in producingbioethanol from alternative sources like microalgae rather thanfeedstock that has minor impact in the daily life [161793]

Bioethanol from microalgae can be produced through thefermentation of the microalgal biomass or directly through cellularreactions [9495]

When considering ethanol production via fermentation the keyis the accumulation of starch which is a potential substrate thatcan reach half of the microalgas cellular dry biomass Microalgalstarch can be extracted by mechanical or enzymatic means andfurther separated by downstream processes incorporating wateror an organic solvent This starch will be hydrolyzed to glucose tobe used in ethanol fermentation [9697] Production mainly differsfrom other crop raw materials in the first steps of the processbecause microalgae will need special concentration harvestingand mechanical disruption systems related with their cellularphysiology and culturing [98]

Microalgae can also excrete ethanol directly through the cellwalls by means of intracellular processes under dark becauseillumination prevents the formation of ethanol except for minoramounts This process which is reported in some microalgae likeChlorococcum littorale [99] Chlamydomonas reinhardtii [8384]Chlamydomonas moewusii [100] Chlorella vulgaris [101] Oscilla-toria limnetica [102] Oscillatoria limosa [99] Gleocapsa alpicola[103] Spirulina platensis [68] Cyanoteche sp [99] covers theanaerobic metabolism in algae where the assimilation and forma-tion of hydrogen carbon dioxide formate acetate ethanol lactateglycerol and butannediol take place [1783] Degradation of intracel-lular starch which is the main endogenous carbon source storedduring aerobic phototrophic metabolism to pyruvate is accomplishedby the EmbdenndashMeyerhofndashParnas and pentose phosphate pathwaysusing pyruvate decarboxylase and alcohol dehydrogenase enzymes[99102] As stated by Gfeller and Gibbs [83] the lack of ethanolproduction by the microalgae cells during illumination is related withthe absence of available reduced pyridine nucleotides with theassumption of active acetaldehyde and alcohol dehydrogenases Twopossible conversion routes for acetyl-CoA to acetate and ethanol canbe followed In the former route half of the acetyl-CoA is converted toacetate by a deacylase while the rest is reduced to ethanol withacetaldehyde as intermediate In the latter route acetyl-CoA is reducedto acetaldehyde that undergoes a dismutation sequence until theformation of acetate and ethanol [8384]

Enhancing direct microalgal bioethanol production by geneticmanipulations is also under consideration Genes from the ethanolproducing bacterium Zymomonas mobilis was transfered intomicroalgae Synechococcus sp aiming to give the ability to utilizethe fixed carbon for direct ethanol excretion to the culture volumethrough the cell walls [93104]

The novelty of the process lies in the separation of producedbioethanol from the culture medium This process eliminates theharvesting step that decreases the energy costs and water usageassociated with the separation processes required for algae har-vesting and fuel extraction [94105]

Besides bioethanol being the main product the remainingmicroalgal biomass may be used to produce biomethane again

Table 4Microalgal hydrogen production

Microalgae Cultivation Process PBR type Culture medium Hydrogen productionprocedure

Time H2 production Refs

Anabaena variabilis (CCAP 14034B)

Continuousndashphotoautotrophic

Lab Stirred (300 mL) Nitrogen free Allen-Arnon

Nitrogen free Allen-Arnon medium

Under vacuum for 15 min Increased light intensity for

5 h at the 6th day ofcultivation

35 days 12ndash14 mL gminus1DW hminus1 [164]

Anabaena variabilis (ATCC 29413) Continuousndashphotoautotrophic

Lab Vial (14 mL) Allen-Arnon(containing Na2MoO4 orNa3VO4 or neither)

Under argon flushing 80ndash100 h

Up to 5 nmol hminus1 mg Chlaminus1 at pH levels of 7ndash9 with Na3VO4 added cultures

[165]

Anabaena sp PCC 7120 (3hydrogenase mutants from PCC7120)

Batchndashphotoautotrophic Lab Sealed polystyrenecuvettes (1 cm light path47 mL capacity)

BG 11 Nitrogen free BG 11 medium Under anaerobic conditions Various light intensities

32ndash40 h Up to 08ndash1 mmol per cuvette (47 mL) [63]

Anabaena sp PCC 7120 and itsmutant AMC 414

Continuousndashphotoautotrophic

Outdoor Tubular-coiled (435 L) BG 11 Nitrogen free BG 11 medium Under argon atmosphere Nitrogen free BG 11 medium Under anaerobic conditions Increased light intensity

7 days 149 mL hminus1Lminus1PBR (373 mL total) with themutant

[166]

Anabaena variabilis (ATCC 29413) Batchndashphotoautotrophic Lab Panel (500 mL capacity) BG 11 50 h Up to 40ndash50 mL [167]

Chlamydomonas reinhardtii(CC124)

BatchndashphotomixotrophicSynchronous andunsynchronous growth

Lab Stirred glass bottles(12L)

TAP TAP-S medium (transferred bycentrifugation)

140 h 102 mL (with 4 h synchronizedcultures)

86 mL (with unsynchronized cultures)

[168]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotomixotrophic Lab Stirred glass bottles(500 mL)

TAP TAP-S medium transfer bycentrifugation

TAP-S medium inoculationby TAP culture (10inoculation)

175 mL Lminus1 (with centrifuged cultures under20ndash40 mE mminus2sminus1 average light intensity)

[87]

Chlamydomonas reinhardtii(CC124)

Continuousndashphotomixotrophic

Lab Stirred glass bottles(1050 mL)

TAP-S (90 mmol sulfateadded)

TAP-S medium two stagechemostat with aerobicstage and anaerobic stage

TAP-S medium TAP medium with limiting

sulfate (10ndash20 mM) Anaerobic conditions Sulfur free medium Anaerobic

4000 h Up to 058 mL hminus1Lminus1PBR [169]

Chlamydomonas reinhardtii (Dang137C mt+ and a nonmotilemutant CC 1036 pf18 mt+)

Batchndashphotomixotrophic-immobilized

Lab Panel (160 mL) TAP (046 mM sulfatereplete)

23 days 45 mL dayminus1 (380 mL total) [170]

Chlamydomonas reinhardtii (Dang137C mt+)

Batch-photoautotrophicmixotrophic andheterotrophic

Lab Flat glass bottles PBR(15 L volume)

HS (CO2 bubbling) TAPwith or without CO2

bubbling

60ndash80 h 11704 mmol Lminus1 (sim28 mL (hL)minus1) inphotoautotrophic cultures

45716 mmol Lminus1 (sim40 mL (hL)minus1) inphotoheterotrophic cultures

09708 mmol Lminus1 (sim69 mL (hL)minus1)inphotomixotrophic cultures

[171]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotoautotrophic Lab Flat glass bottles PBR(15 L)

High salt HS sulfur free medium Argon purging during the

first 24 h of deprivation TAP-S medium Various dilutions Anaerobic conditions

100 h 7173 mL Lminus1 (175 mE mminus2sminus1 lightintensity pH 77)

5272 mL Lminus1 (420 mE mminus2sminus1 lightintensity pH 74)

[172]

Chlamydomonas reinhardtii(CC124)

Semi continuousndashphotomixotrophic

Lab Stirred tank (25 L) TAP 127 days 1108 mL [173]

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic-immobilized

Lab Vials (75 mL) TAP TA-S-P (no sulfate nophosphate) medium

Alginate entrapped

160ndash180 h

0307002 mol mminus2 (125 mmol mgminus1 Chl hminus1) [174]

Batchndashphotomixotrophic Lab Glass bottles (325 mL) TAP 192 h 395 mmol106 cellsminus1 hminus1 with TAP-S [90]

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harvested cells flushed withor without argon

Anaerobic conditions TAP-S or TAP-N DCMU mixed ethanol

addition Dark anaerobic

fermentation

Chlamydomonas reinhardtii(CC124)

34 mmol106 cellsminus1 hminus1 with TAP-N

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Stirred tank (1 255 L) TAP-S TAP-S medium transfer bycentrifugation

Various mixing time Various light energy Scale-up

192 h Max with 122 kJ sminus1 mminus3 light energy and25 min mixing time

[202]

1 L PBR 1537005 mL Lminus1 hminus1

25 L PBR 1327005 mL Lminus1 hminus1

5 L PBR 1027005 mL Lminus1 hminus1

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Tubular (110 L) TAP-S TAP-S medium transfer bycentrifugation

Modified with silicananoparticle to enhancescattering

48 h 3121571789 mL (06 mL Lminus1 hminus1) [203]

Chlorella pyrenoidosa C-101 Batchndashphotoautotrophic Lab Bubble column (650 mL) Modified Bristol Nitrogen flushing under dark forldquo420rdquo h

60ndash65 h 6910minus2 m3 kgminus1 cell [65]

Chlorella vulgaris MSU 01 Batchndashphotomixotrophic Lab Stirred (500 mL) Modified BG11 and MJ Anaerobic conditions Corn stalk as carbon source

in the medium

6ndash7 days 26 mL [175]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Dark incubation Anaerobic nitrogen

atmosphere Addition of specific effectors

(DCMU DCCD DBMIBand CCCP)

Continuous illuminationafterwards

8 h 0339 mL hminus1 Lminus1 (144 mL) based on1106 cells mLminus1 at 15 μM CCCP addedculture after 8 h of illumination

[66]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Sulfur deprive medium Incubation under dark Anaerobic conditions Continuous illumination

afterwards

50 h 11720 nL hminus1 (with seawater-S medium) [67]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Torus (15 L) Defined mineral Dark incubation Anaerobic nitrogen

atmosphere 15 μM CCCP addition Continuous illumination

afterwards

4ndash6 days 720 mL hminus1 (2366770 mL) [176]

Platymonas helgolandica vartsingtaoensis

Batchndashphotoautotrophic Lab Jars (130 mL) F2 Anaerobic Illuminated -S medium Dark CCCPDCMU or both

added medium

25 h 0002 mmol Lminus1 withndashS medium 0160 mmol Lminus1 with CCCP medium 0014 mmol Lminus1 with DCMU medium 0290 mmol Lminus1 with CCCP

+DCMU medium

[89]

Spirulina platensis (NIES-46) Batchndashphotoautotrophic Lab Erlenmeyer flasks(60 mL)

SOT Nitrogen free medium Under dark

20 h 2 mmol mgDWminus1 [68]

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Table

4(con

tinu

ed)

Micro

alga

eCu

ltivation

Pro

cess

PBRtype

Culture

med

ium

Hyd

roge

npro

duction

pro

cedure

Time

H2pro

duction

Refs

Anae

robicco

nditions

Syne

chocystissp

PCC68

03an

dits

mutantNDH-1

complex

defi

cien

tM55

Batch

ndashphotoa

utotrop

hicndash

encapsu

lated

Lab

Vials

(2mL)

BG

11

Nitroge

natmosphere

Under

cycled

lightan

ddark

exposure

5day

s0005

ndash004

5mM

[177

]

Tetraspo

rasp

CU25

51Batch

ndashphotom

ixotrophic

Lab

Vials

TAP(w

itho

rwithou

t05mM

β-mercaptoethan

olfor

24h)

Su

lfuran

dnitroge

ndep

rive

dmed

ium

Argon

flush

edan

aerobic

atmosphere

424

h173ndash61

7mm

olmgminus

1Chlahminus1

[178

]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264252

through anaerobic digestion for electricity generation The carbondioxide and discharged water formed as by-products of thefermentation can be recycled for the microalgae cultivation tofulfill the biorefinery concept [94105]

24 Biomethane

Today agricultural plants or by-products are conventionalsources for renewable biogas production which is mainly amixture of methane (55ndash75) and carbon dioxide (25ndash45) byanaerobic digestion Biomethane from the biogas can be used as afuel for transportation and electricity generation or for heatingpurposes especially in the rural areas [16106107]

Microalgae with their dominancy over crop plants by means ofproductivity per hectare triggered the attention for the production ofbiogas The solar energy converted and stored by the microalgae cellsthrough photosynthesis can be transformed into energy through theanaerobic digestion to produce methane [106108]

Microalgal biomass having high cellular lipid starch andprotein low cellulose and on the other hand the absence of ligningives a reliable and effective anaerobic digestion These specifica-tions make microalgae a good alternative for effective biomethaneproduction compared to the other crop plants [16107108]

Microalgal biomass can be processed anaerobically step by stepwith specialized groups of bacteria [109]

Hydrolyzation of biopolymers to monosaccharides by hydro-lytic bacteria

Fermentation of the monosaccharides to carboxylic acids andalcohols by fermentative bacteria

Conversion of the acids and alcohols to acetate hydrogen andcarbon dioxide by acetogenic bacteria

Conversion of the end products of acetogenic reactions tomethane and carbon dioxide by methanogenic bacteria

Microalgal biomass remaining after the anaerobic digestion canbe further processed to make fertilizers that can add an extra valueto the overall process Also the carbon dioxide portion of theproduced biogas can be recycled again to cultivate the neededmicroalgal biomass for processing [107110ndash112]

A predicted model of microalgae biomass for digestion toproduce electrical and thermal energy discussed the economicprofitability related with technical aspects of the productionsystem The results showed that the microalgae productivityharvesting concentration and usage of high rate anaerobic diges-ters are the key factors for the economic energy production [113]

A life cycle perspective study using a stochastic model indi-cated that when compared with the conventional crops likeswitch grass canola and corn the environmental impact ofmicroalgal biomass production is higher with respect to energydemand greenhouse gas emissions and water use regardless ofcultivation location Only in overall land use and eutrophicationpotential microalgae present favorable results [114] This mayseem to be a disadvantage to produce biomethane from microalgalbiomass but the studies also supported that the integratedprocesses using proper photobioreactors combining microalgaecultivation and waste water treatment systems for biomethaneproduction will help to reduce the environmental impacts result-ing in a competitive and effective production [11416115]

25 Integrated processes

Relations between parameters and the target products (bio-mass lipid hydrogen ethanol) are important in the selection ofthe microalgae for efficient biofuel production As can be followedfrom the tables summarizing the microalgal biofuel productions

Sugars

- Sugarcane juice

- Molasses

- Sugar beet

Starch

- Corn

- Oats

- Wheat

- Sago Palm

- Cassava

- Banana wastes

- Rye

- Barley

- Triticale

- Sorghum

- Algal biomass

Lignocellulosic materials

- Crop residues

- Cellulose wastes

- Hardwood

- Harbaceous biomass

- Softwood

- Municipal solid wastes

Fermentation

- Saccharomyces cerevisiae

- Schizosaccharomyces pombe

- Zymomonas mobilis

- Saccharomyces bayanus

- Pichia stipitis

- Candida shehatae

- Pachysolen tannophilus

- Mucor indicus

- Chalara parvispora

- T thermosaccharolyticum

- T Ethanolicus

- B Stearothermophilus

- C thermohydrosulfuricum

- C thermocellum

- Milling

- Grinding

- ShredingBreaking hemicellulose

chains

- Physical

- Chemical

- Physicochemical

- Biological

Hydrolization -Detoxification

-Neutralization

Sugars

- Hexoses

- Pentoses

Separation and

Concentration

- Distillation

- Rectification

- Dehydration

ETHANOL

Fig 4 Ethanol production from biomass productionSource Adapted from Refs [9398201]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 253

studies focus on the separation of production processes into twomain steps growth mediated and product mediated When con-sidering direct biofuel production the main approach is product

mediated for higher lipid hydrogen or ethanol production Whenconsidering biofuel production integrated with other microorgan-isms (Table 5) the main approach is growth mediated for higher

Table 5Integrated biofuel processes working with microalgae

Microalgae System Product Ref

Chlamydomonas reinhardtii (UTEX 90) Enzymatic treatment of algal biomass and conversion to ethanol by Saccharomyces cerevisiae Ethanol [179]Chlamydomonas reinhardtii (UTEX 90) Hydrothermal acid treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [180]Chlorella vulgaris (IAM C-534) Enzymatic treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [181]Synechococcus leopoliensis (IAMM 6) Fermentation of acid treated saccharified algal biomass by yeast Saccharomyces sake (IFO 2347) Ethanol [97]Chlamydomonas reinhardtii Chlorella vulgaris (macroalgae Undaria pinnatifida) Enzymatic treatment of pre-acid hydrolyzed algal biomass fermentation by 4 different strains of Escherichia coli Ethanol [182]Schizocytrium sp Fermentation of hydrothermal treated algal biomass by E coli KO11 Ethanol [183]Microcystis aeruginosa and Anabaena variabilis Hydrolysis and fermentation of Super Critical fluid pretreated algal biomass by Saccharomyces cerevisiae Ethanol [204]Scenedesmus obliquus Fermentation of algal biomass hydrolysate by Kluyveromyces marxianus IGC 2671 Saccharomyces carlsbergensis

ATCC6269 and Saccharomyces bayanusEthanol [205]

Anabaena sp PCC7120 Fermentation of hydrogen produced residual algal biomass by Enterobacter aerogenes Hydrogen [184]Arthrospira (Spirulina) platensis Nannochloropsis sp and Dunaliella tertilecta Anaerobic fermentation of thermal pretreated algal biomass by immobilized Clostridium acetobutylicum Hydrogen acetone

ethanol butanol[206]

Chlorella vulgaris ESP6 Dark fermentation of acid or alkalineenzyme pretreated algal biomass hydrolysate by Clostridium butyricumCGS5

Hydrogen [207]

Chlorella sp Simultaneous hydrolysis and fermentation of algal biomass by sewage sludge consortia Hydrogen [208]Thalassiosira weissflogii Dark fermentation of algal biomass with the thermophilic bacterium Thermotoga neapolitana Hydrogen [209]Chlamydomonas reinhardtii (IAM C-238) Chlorella pyrenoidosa (IAM C-212) andDunaliella tertiolecta (ATCC 30909)

Fermentation of algal biomass by Lactobacillus amylovorous (ATCC 33620) and Rhodobacter sphaeroides RV Hydrogen [185]

Chlamydomonas reinhardtii (IAM C-238) and Dunaliella tertiolecta (ATCC 30909) Fermentation of algal biomass by Lactobacillus amylovorous and Rhodobium marinum (A-501) mixed culture Hydrogen [186]Chlamydomonas (MGA 161) Fermentation of algal biomass by Rhodovulum sulfidophilum (W-1S) Hydrogen [85]Chlamydomonas reinhardtii (C238) Mixed cultivation of Chlamydomonas reinhardtii (C238) with Rhodospirillum rubrum (NCIB 8255) Hydrogen [187]Scnedesmus sp Fermentation of algal biomass by anaerobic digested sludge Hydrogen [188]Arthrospira maxima Anaerobic digestion of algal biomass by sewage sludge consortia Methane [210]Phaeodactylum tricornutum Anaerobic digestion of algal biomass by potato factory origin anaerobic granular sludge Methane [211]Scenedesmus sp Anaerobic digestion of high pressure thermal pretreated raw and residue (from lipid extraction) algal biomass

and by anaerobic digestor sludgeMethane [212]

Scenedesmus sp Anaerobic digestion of ultrasound and thermal pretreated raw algal biomass by sugar factory origin anaerobicgranular sludge

Methane [213]

Scenedesmus sp Anaerobic digestion of mild thermal pretreated raw algal biomass by sugar factory origin anaerobic granularsludge

Methane [214]

Spirulina platensis Anabaena variabilis and Chlorella sp Processing of algal biomass by an integrated system of methanogenic culture and Rhodobacter capsulatus Methane and hydrogen [189]Spirulina platensis (UTEX 1926) Rhodotorula glutinis (2541) Mixed cultivation of microalgae and yeast using waste water Lipid (biodiesel) [190]Spirulina platensis Using excess CO2 from the ethanol fermentation by Saccharomyces cerevisiae Lipid (biodiesel) [119]Botryococcus braunii (two strains BB763 and BB764) Chlorella vulgaris Chlorellapyrenoidosa

Biodiesel production catalyzed by immobilized Penicillium expansum lipase and Candida antarctica lipase B(Novozym 435)

Lipid (biodiesel) [191]

Chlorella vulgaris (21111B) Anaerobic digestion of algal biomass by sewage sludge origin methanogenic culture Methane [112]Chlorella sp and Scenedesmus Anaerobic digestion of algal biomass by sewage sludge culture Methane [106]Chlorella sp Anaerobic digestion of algal biomass by sludge culture Methane [192]Arthrospira platensis Chlamydomonas reinhardtii Chlorella kessleri Dunaliellasalina Euglena gracilis and Scenedesmus obliquus

Anaerobic digestion of algal biomass by sewage sludge culture Methane [107]

Spirulina maxima Anaerobic digestion of algal biomass by sewage sludge culture Methane [193]Chlorella sp and Scenedesmus Anaerobic codigestion of algal biomass with waste paper by methanogenic culture Methane [194]Tetraselmis Anaerobic digestion of algal biomass by methanogenic culture Methane [195]Chlorococcum sp Anaerobic treatment of distillery waste with algal biomass by acidogenicmethanogenic culture Methane [196]Phaeodactylum tricornutum (CCAP10551) Anaerobic digestion of algal biomass by granular seed sludge from digester treating potato processing waste

water dominated by Methanosaeta sp and Methanosarcina spMethane [197]

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 255

biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264256

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

SSOncel

Renew

ableand

SustainableEnergy

Review

s26

(2013)241

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 259

technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

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[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264262

[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 8: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264248

Conventional technology of chemical catalysis has some con-straints due to the environmental problems related with soapformation and energy demand due to the downstream processesto recover glycerol and catalysts [262831]

Biological catalysis has some advantages over the chemicalcatalysis including lower energy demand moderate reaction con-ditions lower alcohol to oil ratio easier product recovery and highconversion [3132]

Lipases are the key biocatalysts that are used in biodieselproduction Major producer microorganisms for lipases are Aspergil-lus niger Aspergillus oryzae Bacillus pumilis Burkholderla cepaciaCandida antarctica Candida cylindracea Candida lipolytica Candidaparalipolytica Candida rugosa Chromobacterium viscosum Enterobac-ter aerogenes Eremothecium ashbyii Escherichia coli Geotrichumcandidum Mucor miehei Penicillium cyclopium Penicillium expansumPenicillium restrictum Pseudomonas cepacia Pseudomonas fluorescensPseudomonas fragi Rhizopus arrhizus Rhizopus delemar Rhyzomucormiehei Rhizopus oryzae Saccharomyces cerevisiae and Thermomyceslanuginosus which are also commercially important to meet theneeds of the large scale biodiesel processes [3334]

Main bottlenecks of this process include high cost of enzymelow yield due to inactivation longer reaction time slower reactionrate and the amount of water and organic solvents in the reactionmixture [2532]

The limitations in the biocatalysis are managed via the immo-bilization of the lipases in packed bed reactors to prevent washoutand inactivation [35] using whole cell immobilization [26] ionicliquids in enzyme catalysis [3136] genetic modifications andrecombinant microorganisms to enhance the efficiency and theproduction of the enzyme [26] alternative acyl acceptors [37]stepwise processes [3839] moderate polar solvents [40] non-catalytic methods under supercritical conditions [4142] and highpressure processes to stabilize the enzymes [4344]

From the economical point of view which is also importantchemical catalysis is reported to be cheaper than biologicalcatalysis But the modifications like using immobilized biocatalystsand the enhanced reuse can serve a competitive cost compared tothe chemical catalysts [45]

Numerous approaches are still in progress for the optimizationof the biodiesel production process adaptable to different feedtypes compositions and downstream requirements One of thenovel processes mentioned in recent studies is the ldquoMcgyan Processrdquothat consists of a continuous fixed bed reactor that can producebiodiesel using a metal oxide based catalyst The process is analternative method for continuous transesterification and can use awide variety of feedstock does not consume the catalyst reducesthe reaction time from hours to seconds and does not use water ordangerous chemicals [164647] Treatment of the lipids extractedfrom Dunaliella tertiolecta and Nannochloropsis oculata with Mcgyanprocess to produce biodiesel reached up to 85 in the conversion oftriacylglycerides and free fatty acids to alkyl esters [48]

Alternatively by shifting the production route microalgal oilscan be used to produce ldquogreen dieselrdquo by a process known ascatalytic hydroprocessing The basic difference of this with trans-esterification is the usage of hydrogen rather than the alcohol Alsothe by-products like propane water and carbon dioxide differfrom glycerol of transesterification [816] Green diesel has super-iority over biodiesel with its lower oxygen constitution similar tothe petroleum derived fuels with a near zero oxygen content Theprimary goal of the processes is to produce a minimized oxygencontaining green diesel with maximized final energy content[816] Also because of the high paraffinic hydrocarbon contentgreen diesel has higher cetane numbers and energy content onmass basis compared to biodiesel Using the microalgal oils forgreen diesel will be advantageous because of the applicationpotential in the conventional petroleum refinery systems with

existing infrastructure and the by-products (H2O and CO2) can berecycled to be used in the microalgae cultivation again

With the rapid progress in the area of genetic engineering theresearchers can now present the genome sequences of microalgaefor example a lipid producing microalgae specie that has potentialin biofuel production ie Nannochloropsis gaditana genome isnewly finalized and may become a model organism like Chlamy-domonas reinhardtii Chlorella variabilis Micromonas pusila Ostreo-coccus tauri Ostreococcus lucimarinus Thalassiosira psudonanaEmiliana huxleyii Fragilariopsis cylindrus Aerococcus aophageffe-rens Cyanidioschyzon merolae and Phaeodactylum tricornutum withcompleted genomes [4950] By understanding these model micro-organisms in molecular basis we can have the chance to improveproductivities in future applications

The ultimate idea was the excretion of the oils from themicroalgae cells without the need of extraction step This ideawas supported with the studies focusing on Escherichia coli andSaccharomyces cerevisiae to excrete lipids through membraneswith genetic engineering tools [5152]

22 Biohydrogen

Hydrogen with its unique properties is accepted to be arenewable sustainable and environmentally friendly energy car-rier that serve as one of the most promising alternative solution toovercome the growing environmental concerns considering thefuture energy demands [5354]

Today there are various conventional as well as novel strategiesto produce hydrogen from fossil fuels (steam reforming plasmareforming thermal cracking gasification) biomass (pyrolysismicrobial conversion syngas conversion supercritical conversiongasification) and water (photolysis thermolysis electrolysis)incorporating chemical and biological processes [272955] Evenif the hydrogen production is dominated by the chemical pro-cesses using fossil fuels biological processes started to get moreattention since the first studies in the 1920s [56ndash58]

The metabolic routes for biohydrogen production differ accord-ing to the microorganism [2759]

Microalgae

(a) Direct photolysis 2H2O-light-2H2+O2

(b) Indirect photolysis(1) 12H2O+6CO2-light-C6H12O6+6O2

(2) C6H12O6+12H2O-12H2+6CO2Photosynthetic bacteria(a) Photofermentation CH3COOH+2H2O-light-4H2+2CO2

(b) Water-gas shift CO+H2O-H2+CO2Anaerobic bacteria Dark fermentationC6H12O6+2H2O-4H2+2CO2+2CH3COOH

Related with their photosynthetic productivity and light utili-zation efficiency microalgae can perform special biochemical andphotochemical reactions with minimum requirements that makehydrogen production possible under aerobic and anaerobic envir-onments [60ndash62]

Microalga like Anabaena sp [6364] Chlorella pyrenoidosa [65]Chlorella vulgaris [66] Platymonas subcordiformis [6667] Spirulinaplatensis [68] and especially Chlamydomonas reinhardtii [6970] getattention in biohydrogen production

Microalgae use two classes of oxygen sensitive metalloenzymesnitrogenases and hydrogenases that are closely related with thefinal biohydrogen generation process in photosynthesis [6371]

There are several types of hydrogenases like the hup-encodedNiFe-uptake hydrogenases hox-encoded NiFe-bidirectional hydro-genases FeFe hydrogenases NiFeSe-bidirectional hydrogenases

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 249

and Fe-only hydrogenases utilized by bacteria and microalgae Onthe other hand nitrogenases of purple non-sulfur bacteria andheterocyst microalgae can be classified by their metal cofactor asmolybdenum iron and vanadium types [7273]

Nitrogenase is the part of the biological nitrogen fixation andhydrogenase is capable to catalyze hydrogen consuming reactionsBiohydrogen production based on these enzymes differs in energyconsumption Hydrogenase mediated reactions are about threetimes more efficient than nitrogenase catalyzed reactions based onspent energy in the form of ATP On the other hand nitrogenasesare relatively less sensitive to oxygen compared to hydrogenases[74ndash76] Relatively or not because both enzymes are sensitive tooxygen it is important to control culture conditions for optimalhydrogen production

Microalgal biohydrogen production can take place duringphotosynthesis from water by the two photosystems dark fer-mentation of the reduced carbon produced by photosynthesis andphotofermentation by the enzymatic oxidation of intracellularreductants derived from fermentation [77ndash80]

Even if the studies on microalgal biohydrogen started in the 1930s[568182] it was shown that the production can be achieved by theinactivation of photosynthetic water oxidizing activity catalyzed bythe reaction center of photosystem two (PSII) [83ndash85] the productiv-ities could not reach to meaningful levels until there was a novelprotocol depending on sulfur deprivation [69] This protocol dependson the succession of photosynthetic reactions in which oxygenproduction and carbon accumulation take place and anaerobic photo-reactions through which the consumption of stored photosyntheticcellular metabolites for biohydrogen generation take place Sulfurdeprivation triggers the conversion of PSII centers to an intermediatein the PSII repair cycle in other words from a QB-reducing to aQB-nonreducing form resulting in the decrease of photosyntheticoxygen evolution capacity [86ndash88]

Compared to the other methods like using inhibitors (DBMIBDCMU SAL C1-CCP etc) or alternating lightdark cycle the removalof sulfate from the growth medium achieves a reversible inactiva-tion with sustainable and increased hydrogen production [83ndash85]

Most of the recent studies focused on the two stage sulfurdeprivation protocol however as summarized by some of theexample studies from batch to continuous processes with variousprocedures the use of different microalgae is a good sign of theprogress towards the future (Table 4) But again some microalgaelike Platymonas subcordiformis Platymonas helgolandica or Chla-mydomonas moewusii are not sensitive to sulfur deprivation aswell as Chlamydomonas reinhardtii so utilization of inhibitors andnitrogen starvation enhance the hydrogen production [8990]

Also the outdoor studies point out another bottleneck in theproductions Even if the applications in lab scale are givingpromising results outdoor cultures still cannot reach the compar-able levels Microalgae cells have problems to tolerate the lightinhibition and sulfur deprivation when exposed to direct sunlightoutdoors They need to be acclimated to light before the hydrogenproduction phase [91]

Besides the studies on the enhancement of the biohydrogenproduction focusing on culture techniques like utilization of immobi-lized microalgae or stressed cultivations with regard to light andmedium components the progress in genetic engineering to improveproduction levels focuses on engineering truncated antennas of thespecies for better sunlight utilization outdoors without inhibition orengineering oxygen tolerant species that can produce hydrogen inaerobic conditions which is still under investigation [7392]

23 Bioethanol

Bioethanol may be considered as an alternative clean burningfuel because of its environmentally friendly combustion products

with low greenhouse gas effect relative to fossil fuels Todaycommercial bioethanol production is mainly from agriculturalstocks and raw materials like corn rice wheat cassava sugarcane sugar beet and sweet sorghum through biochemical orthermochemical processes [161793] Even though the route ofproduction depends on the raw material it can be summarized asthe breaking of the biomaterial to simple sugars that furtherfermented using alcohol producing microorganisms The producedethanol later separated and concentrated through downstreamprocesses (Fig 4)

Facing the conflict of global energy and food demand therehave been increasing interest and worldwide studies in producingbioethanol from alternative sources like microalgae rather thanfeedstock that has minor impact in the daily life [161793]

Bioethanol from microalgae can be produced through thefermentation of the microalgal biomass or directly through cellularreactions [9495]

When considering ethanol production via fermentation the keyis the accumulation of starch which is a potential substrate thatcan reach half of the microalgas cellular dry biomass Microalgalstarch can be extracted by mechanical or enzymatic means andfurther separated by downstream processes incorporating wateror an organic solvent This starch will be hydrolyzed to glucose tobe used in ethanol fermentation [9697] Production mainly differsfrom other crop raw materials in the first steps of the processbecause microalgae will need special concentration harvestingand mechanical disruption systems related with their cellularphysiology and culturing [98]

Microalgae can also excrete ethanol directly through the cellwalls by means of intracellular processes under dark becauseillumination prevents the formation of ethanol except for minoramounts This process which is reported in some microalgae likeChlorococcum littorale [99] Chlamydomonas reinhardtii [8384]Chlamydomonas moewusii [100] Chlorella vulgaris [101] Oscilla-toria limnetica [102] Oscillatoria limosa [99] Gleocapsa alpicola[103] Spirulina platensis [68] Cyanoteche sp [99] covers theanaerobic metabolism in algae where the assimilation and forma-tion of hydrogen carbon dioxide formate acetate ethanol lactateglycerol and butannediol take place [1783] Degradation of intracel-lular starch which is the main endogenous carbon source storedduring aerobic phototrophic metabolism to pyruvate is accomplishedby the EmbdenndashMeyerhofndashParnas and pentose phosphate pathwaysusing pyruvate decarboxylase and alcohol dehydrogenase enzymes[99102] As stated by Gfeller and Gibbs [83] the lack of ethanolproduction by the microalgae cells during illumination is related withthe absence of available reduced pyridine nucleotides with theassumption of active acetaldehyde and alcohol dehydrogenases Twopossible conversion routes for acetyl-CoA to acetate and ethanol canbe followed In the former route half of the acetyl-CoA is converted toacetate by a deacylase while the rest is reduced to ethanol withacetaldehyde as intermediate In the latter route acetyl-CoA is reducedto acetaldehyde that undergoes a dismutation sequence until theformation of acetate and ethanol [8384]

Enhancing direct microalgal bioethanol production by geneticmanipulations is also under consideration Genes from the ethanolproducing bacterium Zymomonas mobilis was transfered intomicroalgae Synechococcus sp aiming to give the ability to utilizethe fixed carbon for direct ethanol excretion to the culture volumethrough the cell walls [93104]

The novelty of the process lies in the separation of producedbioethanol from the culture medium This process eliminates theharvesting step that decreases the energy costs and water usageassociated with the separation processes required for algae har-vesting and fuel extraction [94105]

Besides bioethanol being the main product the remainingmicroalgal biomass may be used to produce biomethane again

Table 4Microalgal hydrogen production

Microalgae Cultivation Process PBR type Culture medium Hydrogen productionprocedure

Time H2 production Refs

Anabaena variabilis (CCAP 14034B)

Continuousndashphotoautotrophic

Lab Stirred (300 mL) Nitrogen free Allen-Arnon

Nitrogen free Allen-Arnon medium

Under vacuum for 15 min Increased light intensity for

5 h at the 6th day ofcultivation

35 days 12ndash14 mL gminus1DW hminus1 [164]

Anabaena variabilis (ATCC 29413) Continuousndashphotoautotrophic

Lab Vial (14 mL) Allen-Arnon(containing Na2MoO4 orNa3VO4 or neither)

Under argon flushing 80ndash100 h

Up to 5 nmol hminus1 mg Chlaminus1 at pH levels of 7ndash9 with Na3VO4 added cultures

[165]

Anabaena sp PCC 7120 (3hydrogenase mutants from PCC7120)

Batchndashphotoautotrophic Lab Sealed polystyrenecuvettes (1 cm light path47 mL capacity)

BG 11 Nitrogen free BG 11 medium Under anaerobic conditions Various light intensities

32ndash40 h Up to 08ndash1 mmol per cuvette (47 mL) [63]

Anabaena sp PCC 7120 and itsmutant AMC 414

Continuousndashphotoautotrophic

Outdoor Tubular-coiled (435 L) BG 11 Nitrogen free BG 11 medium Under argon atmosphere Nitrogen free BG 11 medium Under anaerobic conditions Increased light intensity

7 days 149 mL hminus1Lminus1PBR (373 mL total) with themutant

[166]

Anabaena variabilis (ATCC 29413) Batchndashphotoautotrophic Lab Panel (500 mL capacity) BG 11 50 h Up to 40ndash50 mL [167]

Chlamydomonas reinhardtii(CC124)

BatchndashphotomixotrophicSynchronous andunsynchronous growth

Lab Stirred glass bottles(12L)

TAP TAP-S medium (transferred bycentrifugation)

140 h 102 mL (with 4 h synchronizedcultures)

86 mL (with unsynchronized cultures)

[168]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotomixotrophic Lab Stirred glass bottles(500 mL)

TAP TAP-S medium transfer bycentrifugation

TAP-S medium inoculationby TAP culture (10inoculation)

175 mL Lminus1 (with centrifuged cultures under20ndash40 mE mminus2sminus1 average light intensity)

[87]

Chlamydomonas reinhardtii(CC124)

Continuousndashphotomixotrophic

Lab Stirred glass bottles(1050 mL)

TAP-S (90 mmol sulfateadded)

TAP-S medium two stagechemostat with aerobicstage and anaerobic stage

TAP-S medium TAP medium with limiting

sulfate (10ndash20 mM) Anaerobic conditions Sulfur free medium Anaerobic

4000 h Up to 058 mL hminus1Lminus1PBR [169]

Chlamydomonas reinhardtii (Dang137C mt+ and a nonmotilemutant CC 1036 pf18 mt+)

Batchndashphotomixotrophic-immobilized

Lab Panel (160 mL) TAP (046 mM sulfatereplete)

23 days 45 mL dayminus1 (380 mL total) [170]

Chlamydomonas reinhardtii (Dang137C mt+)

Batch-photoautotrophicmixotrophic andheterotrophic

Lab Flat glass bottles PBR(15 L volume)

HS (CO2 bubbling) TAPwith or without CO2

bubbling

60ndash80 h 11704 mmol Lminus1 (sim28 mL (hL)minus1) inphotoautotrophic cultures

45716 mmol Lminus1 (sim40 mL (hL)minus1) inphotoheterotrophic cultures

09708 mmol Lminus1 (sim69 mL (hL)minus1)inphotomixotrophic cultures

[171]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotoautotrophic Lab Flat glass bottles PBR(15 L)

High salt HS sulfur free medium Argon purging during the

first 24 h of deprivation TAP-S medium Various dilutions Anaerobic conditions

100 h 7173 mL Lminus1 (175 mE mminus2sminus1 lightintensity pH 77)

5272 mL Lminus1 (420 mE mminus2sminus1 lightintensity pH 74)

[172]

Chlamydomonas reinhardtii(CC124)

Semi continuousndashphotomixotrophic

Lab Stirred tank (25 L) TAP 127 days 1108 mL [173]

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic-immobilized

Lab Vials (75 mL) TAP TA-S-P (no sulfate nophosphate) medium

Alginate entrapped

160ndash180 h

0307002 mol mminus2 (125 mmol mgminus1 Chl hminus1) [174]

Batchndashphotomixotrophic Lab Glass bottles (325 mL) TAP 192 h 395 mmol106 cellsminus1 hminus1 with TAP-S [90]

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ndash264250

harvested cells flushed withor without argon

Anaerobic conditions TAP-S or TAP-N DCMU mixed ethanol

addition Dark anaerobic

fermentation

Chlamydomonas reinhardtii(CC124)

34 mmol106 cellsminus1 hminus1 with TAP-N

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Stirred tank (1 255 L) TAP-S TAP-S medium transfer bycentrifugation

Various mixing time Various light energy Scale-up

192 h Max with 122 kJ sminus1 mminus3 light energy and25 min mixing time

[202]

1 L PBR 1537005 mL Lminus1 hminus1

25 L PBR 1327005 mL Lminus1 hminus1

5 L PBR 1027005 mL Lminus1 hminus1

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Tubular (110 L) TAP-S TAP-S medium transfer bycentrifugation

Modified with silicananoparticle to enhancescattering

48 h 3121571789 mL (06 mL Lminus1 hminus1) [203]

Chlorella pyrenoidosa C-101 Batchndashphotoautotrophic Lab Bubble column (650 mL) Modified Bristol Nitrogen flushing under dark forldquo420rdquo h

60ndash65 h 6910minus2 m3 kgminus1 cell [65]

Chlorella vulgaris MSU 01 Batchndashphotomixotrophic Lab Stirred (500 mL) Modified BG11 and MJ Anaerobic conditions Corn stalk as carbon source

in the medium

6ndash7 days 26 mL [175]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Dark incubation Anaerobic nitrogen

atmosphere Addition of specific effectors

(DCMU DCCD DBMIBand CCCP)

Continuous illuminationafterwards

8 h 0339 mL hminus1 Lminus1 (144 mL) based on1106 cells mLminus1 at 15 μM CCCP addedculture after 8 h of illumination

[66]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Sulfur deprive medium Incubation under dark Anaerobic conditions Continuous illumination

afterwards

50 h 11720 nL hminus1 (with seawater-S medium) [67]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Torus (15 L) Defined mineral Dark incubation Anaerobic nitrogen

atmosphere 15 μM CCCP addition Continuous illumination

afterwards

4ndash6 days 720 mL hminus1 (2366770 mL) [176]

Platymonas helgolandica vartsingtaoensis

Batchndashphotoautotrophic Lab Jars (130 mL) F2 Anaerobic Illuminated -S medium Dark CCCPDCMU or both

added medium

25 h 0002 mmol Lminus1 withndashS medium 0160 mmol Lminus1 with CCCP medium 0014 mmol Lminus1 with DCMU medium 0290 mmol Lminus1 with CCCP

+DCMU medium

[89]

Spirulina platensis (NIES-46) Batchndashphotoautotrophic Lab Erlenmeyer flasks(60 mL)

SOT Nitrogen free medium Under dark

20 h 2 mmol mgDWminus1 [68]

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Table

4(con

tinu

ed)

Micro

alga

eCu

ltivation

Pro

cess

PBRtype

Culture

med

ium

Hyd

roge

npro

duction

pro

cedure

Time

H2pro

duction

Refs

Anae

robicco

nditions

Syne

chocystissp

PCC68

03an

dits

mutantNDH-1

complex

defi

cien

tM55

Batch

ndashphotoa

utotrop

hicndash

encapsu

lated

Lab

Vials

(2mL)

BG

11

Nitroge

natmosphere

Under

cycled

lightan

ddark

exposure

5day

s0005

ndash004

5mM

[177

]

Tetraspo

rasp

CU25

51Batch

ndashphotom

ixotrophic

Lab

Vials

TAP(w

itho

rwithou

t05mM

β-mercaptoethan

olfor

24h)

Su

lfuran

dnitroge

ndep

rive

dmed

ium

Argon

flush

edan

aerobic

atmosphere

424

h173ndash61

7mm

olmgminus

1Chlahminus1

[178

]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264252

through anaerobic digestion for electricity generation The carbondioxide and discharged water formed as by-products of thefermentation can be recycled for the microalgae cultivation tofulfill the biorefinery concept [94105]

24 Biomethane

Today agricultural plants or by-products are conventionalsources for renewable biogas production which is mainly amixture of methane (55ndash75) and carbon dioxide (25ndash45) byanaerobic digestion Biomethane from the biogas can be used as afuel for transportation and electricity generation or for heatingpurposes especially in the rural areas [16106107]

Microalgae with their dominancy over crop plants by means ofproductivity per hectare triggered the attention for the production ofbiogas The solar energy converted and stored by the microalgae cellsthrough photosynthesis can be transformed into energy through theanaerobic digestion to produce methane [106108]

Microalgal biomass having high cellular lipid starch andprotein low cellulose and on the other hand the absence of ligningives a reliable and effective anaerobic digestion These specifica-tions make microalgae a good alternative for effective biomethaneproduction compared to the other crop plants [16107108]

Microalgal biomass can be processed anaerobically step by stepwith specialized groups of bacteria [109]

Hydrolyzation of biopolymers to monosaccharides by hydro-lytic bacteria

Fermentation of the monosaccharides to carboxylic acids andalcohols by fermentative bacteria

Conversion of the acids and alcohols to acetate hydrogen andcarbon dioxide by acetogenic bacteria

Conversion of the end products of acetogenic reactions tomethane and carbon dioxide by methanogenic bacteria

Microalgal biomass remaining after the anaerobic digestion canbe further processed to make fertilizers that can add an extra valueto the overall process Also the carbon dioxide portion of theproduced biogas can be recycled again to cultivate the neededmicroalgal biomass for processing [107110ndash112]

A predicted model of microalgae biomass for digestion toproduce electrical and thermal energy discussed the economicprofitability related with technical aspects of the productionsystem The results showed that the microalgae productivityharvesting concentration and usage of high rate anaerobic diges-ters are the key factors for the economic energy production [113]

A life cycle perspective study using a stochastic model indi-cated that when compared with the conventional crops likeswitch grass canola and corn the environmental impact ofmicroalgal biomass production is higher with respect to energydemand greenhouse gas emissions and water use regardless ofcultivation location Only in overall land use and eutrophicationpotential microalgae present favorable results [114] This mayseem to be a disadvantage to produce biomethane from microalgalbiomass but the studies also supported that the integratedprocesses using proper photobioreactors combining microalgaecultivation and waste water treatment systems for biomethaneproduction will help to reduce the environmental impacts result-ing in a competitive and effective production [11416115]

25 Integrated processes

Relations between parameters and the target products (bio-mass lipid hydrogen ethanol) are important in the selection ofthe microalgae for efficient biofuel production As can be followedfrom the tables summarizing the microalgal biofuel productions

Sugars

- Sugarcane juice

- Molasses

- Sugar beet

Starch

- Corn

- Oats

- Wheat

- Sago Palm

- Cassava

- Banana wastes

- Rye

- Barley

- Triticale

- Sorghum

- Algal biomass

Lignocellulosic materials

- Crop residues

- Cellulose wastes

- Hardwood

- Harbaceous biomass

- Softwood

- Municipal solid wastes

Fermentation

- Saccharomyces cerevisiae

- Schizosaccharomyces pombe

- Zymomonas mobilis

- Saccharomyces bayanus

- Pichia stipitis

- Candida shehatae

- Pachysolen tannophilus

- Mucor indicus

- Chalara parvispora

- T thermosaccharolyticum

- T Ethanolicus

- B Stearothermophilus

- C thermohydrosulfuricum

- C thermocellum

- Milling

- Grinding

- ShredingBreaking hemicellulose

chains

- Physical

- Chemical

- Physicochemical

- Biological

Hydrolization -Detoxification

-Neutralization

Sugars

- Hexoses

- Pentoses

Separation and

Concentration

- Distillation

- Rectification

- Dehydration

ETHANOL

Fig 4 Ethanol production from biomass productionSource Adapted from Refs [9398201]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 253

studies focus on the separation of production processes into twomain steps growth mediated and product mediated When con-sidering direct biofuel production the main approach is product

mediated for higher lipid hydrogen or ethanol production Whenconsidering biofuel production integrated with other microorgan-isms (Table 5) the main approach is growth mediated for higher

Table 5Integrated biofuel processes working with microalgae

Microalgae System Product Ref

Chlamydomonas reinhardtii (UTEX 90) Enzymatic treatment of algal biomass and conversion to ethanol by Saccharomyces cerevisiae Ethanol [179]Chlamydomonas reinhardtii (UTEX 90) Hydrothermal acid treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [180]Chlorella vulgaris (IAM C-534) Enzymatic treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [181]Synechococcus leopoliensis (IAMM 6) Fermentation of acid treated saccharified algal biomass by yeast Saccharomyces sake (IFO 2347) Ethanol [97]Chlamydomonas reinhardtii Chlorella vulgaris (macroalgae Undaria pinnatifida) Enzymatic treatment of pre-acid hydrolyzed algal biomass fermentation by 4 different strains of Escherichia coli Ethanol [182]Schizocytrium sp Fermentation of hydrothermal treated algal biomass by E coli KO11 Ethanol [183]Microcystis aeruginosa and Anabaena variabilis Hydrolysis and fermentation of Super Critical fluid pretreated algal biomass by Saccharomyces cerevisiae Ethanol [204]Scenedesmus obliquus Fermentation of algal biomass hydrolysate by Kluyveromyces marxianus IGC 2671 Saccharomyces carlsbergensis

ATCC6269 and Saccharomyces bayanusEthanol [205]

Anabaena sp PCC7120 Fermentation of hydrogen produced residual algal biomass by Enterobacter aerogenes Hydrogen [184]Arthrospira (Spirulina) platensis Nannochloropsis sp and Dunaliella tertilecta Anaerobic fermentation of thermal pretreated algal biomass by immobilized Clostridium acetobutylicum Hydrogen acetone

ethanol butanol[206]

Chlorella vulgaris ESP6 Dark fermentation of acid or alkalineenzyme pretreated algal biomass hydrolysate by Clostridium butyricumCGS5

Hydrogen [207]

Chlorella sp Simultaneous hydrolysis and fermentation of algal biomass by sewage sludge consortia Hydrogen [208]Thalassiosira weissflogii Dark fermentation of algal biomass with the thermophilic bacterium Thermotoga neapolitana Hydrogen [209]Chlamydomonas reinhardtii (IAM C-238) Chlorella pyrenoidosa (IAM C-212) andDunaliella tertiolecta (ATCC 30909)

Fermentation of algal biomass by Lactobacillus amylovorous (ATCC 33620) and Rhodobacter sphaeroides RV Hydrogen [185]

Chlamydomonas reinhardtii (IAM C-238) and Dunaliella tertiolecta (ATCC 30909) Fermentation of algal biomass by Lactobacillus amylovorous and Rhodobium marinum (A-501) mixed culture Hydrogen [186]Chlamydomonas (MGA 161) Fermentation of algal biomass by Rhodovulum sulfidophilum (W-1S) Hydrogen [85]Chlamydomonas reinhardtii (C238) Mixed cultivation of Chlamydomonas reinhardtii (C238) with Rhodospirillum rubrum (NCIB 8255) Hydrogen [187]Scnedesmus sp Fermentation of algal biomass by anaerobic digested sludge Hydrogen [188]Arthrospira maxima Anaerobic digestion of algal biomass by sewage sludge consortia Methane [210]Phaeodactylum tricornutum Anaerobic digestion of algal biomass by potato factory origin anaerobic granular sludge Methane [211]Scenedesmus sp Anaerobic digestion of high pressure thermal pretreated raw and residue (from lipid extraction) algal biomass

and by anaerobic digestor sludgeMethane [212]

Scenedesmus sp Anaerobic digestion of ultrasound and thermal pretreated raw algal biomass by sugar factory origin anaerobicgranular sludge

Methane [213]

Scenedesmus sp Anaerobic digestion of mild thermal pretreated raw algal biomass by sugar factory origin anaerobic granularsludge

Methane [214]

Spirulina platensis Anabaena variabilis and Chlorella sp Processing of algal biomass by an integrated system of methanogenic culture and Rhodobacter capsulatus Methane and hydrogen [189]Spirulina platensis (UTEX 1926) Rhodotorula glutinis (2541) Mixed cultivation of microalgae and yeast using waste water Lipid (biodiesel) [190]Spirulina platensis Using excess CO2 from the ethanol fermentation by Saccharomyces cerevisiae Lipid (biodiesel) [119]Botryococcus braunii (two strains BB763 and BB764) Chlorella vulgaris Chlorellapyrenoidosa

Biodiesel production catalyzed by immobilized Penicillium expansum lipase and Candida antarctica lipase B(Novozym 435)

Lipid (biodiesel) [191]

Chlorella vulgaris (21111B) Anaerobic digestion of algal biomass by sewage sludge origin methanogenic culture Methane [112]Chlorella sp and Scenedesmus Anaerobic digestion of algal biomass by sewage sludge culture Methane [106]Chlorella sp Anaerobic digestion of algal biomass by sludge culture Methane [192]Arthrospira platensis Chlamydomonas reinhardtii Chlorella kessleri Dunaliellasalina Euglena gracilis and Scenedesmus obliquus

Anaerobic digestion of algal biomass by sewage sludge culture Methane [107]

Spirulina maxima Anaerobic digestion of algal biomass by sewage sludge culture Methane [193]Chlorella sp and Scenedesmus Anaerobic codigestion of algal biomass with waste paper by methanogenic culture Methane [194]Tetraselmis Anaerobic digestion of algal biomass by methanogenic culture Methane [195]Chlorococcum sp Anaerobic treatment of distillery waste with algal biomass by acidogenicmethanogenic culture Methane [196]Phaeodactylum tricornutum (CCAP10551) Anaerobic digestion of algal biomass by granular seed sludge from digester treating potato processing waste

water dominated by Methanosaeta sp and Methanosarcina spMethane [197]

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biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

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technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

[1] EIA (US Energy Information Administration) International Energy Outlook2010 Washington DC 20585 US 2010 langwwweiagovoiafieoindexhtmlrang

[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264262

[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 9: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 249

and Fe-only hydrogenases utilized by bacteria and microalgae Onthe other hand nitrogenases of purple non-sulfur bacteria andheterocyst microalgae can be classified by their metal cofactor asmolybdenum iron and vanadium types [7273]

Nitrogenase is the part of the biological nitrogen fixation andhydrogenase is capable to catalyze hydrogen consuming reactionsBiohydrogen production based on these enzymes differs in energyconsumption Hydrogenase mediated reactions are about threetimes more efficient than nitrogenase catalyzed reactions based onspent energy in the form of ATP On the other hand nitrogenasesare relatively less sensitive to oxygen compared to hydrogenases[74ndash76] Relatively or not because both enzymes are sensitive tooxygen it is important to control culture conditions for optimalhydrogen production

Microalgal biohydrogen production can take place duringphotosynthesis from water by the two photosystems dark fer-mentation of the reduced carbon produced by photosynthesis andphotofermentation by the enzymatic oxidation of intracellularreductants derived from fermentation [77ndash80]

Even if the studies on microalgal biohydrogen started in the 1930s[568182] it was shown that the production can be achieved by theinactivation of photosynthetic water oxidizing activity catalyzed bythe reaction center of photosystem two (PSII) [83ndash85] the productiv-ities could not reach to meaningful levels until there was a novelprotocol depending on sulfur deprivation [69] This protocol dependson the succession of photosynthetic reactions in which oxygenproduction and carbon accumulation take place and anaerobic photo-reactions through which the consumption of stored photosyntheticcellular metabolites for biohydrogen generation take place Sulfurdeprivation triggers the conversion of PSII centers to an intermediatein the PSII repair cycle in other words from a QB-reducing to aQB-nonreducing form resulting in the decrease of photosyntheticoxygen evolution capacity [86ndash88]

Compared to the other methods like using inhibitors (DBMIBDCMU SAL C1-CCP etc) or alternating lightdark cycle the removalof sulfate from the growth medium achieves a reversible inactiva-tion with sustainable and increased hydrogen production [83ndash85]

Most of the recent studies focused on the two stage sulfurdeprivation protocol however as summarized by some of theexample studies from batch to continuous processes with variousprocedures the use of different microalgae is a good sign of theprogress towards the future (Table 4) But again some microalgaelike Platymonas subcordiformis Platymonas helgolandica or Chla-mydomonas moewusii are not sensitive to sulfur deprivation aswell as Chlamydomonas reinhardtii so utilization of inhibitors andnitrogen starvation enhance the hydrogen production [8990]

Also the outdoor studies point out another bottleneck in theproductions Even if the applications in lab scale are givingpromising results outdoor cultures still cannot reach the compar-able levels Microalgae cells have problems to tolerate the lightinhibition and sulfur deprivation when exposed to direct sunlightoutdoors They need to be acclimated to light before the hydrogenproduction phase [91]

Besides the studies on the enhancement of the biohydrogenproduction focusing on culture techniques like utilization of immobi-lized microalgae or stressed cultivations with regard to light andmedium components the progress in genetic engineering to improveproduction levels focuses on engineering truncated antennas of thespecies for better sunlight utilization outdoors without inhibition orengineering oxygen tolerant species that can produce hydrogen inaerobic conditions which is still under investigation [7392]

23 Bioethanol

Bioethanol may be considered as an alternative clean burningfuel because of its environmentally friendly combustion products

with low greenhouse gas effect relative to fossil fuels Todaycommercial bioethanol production is mainly from agriculturalstocks and raw materials like corn rice wheat cassava sugarcane sugar beet and sweet sorghum through biochemical orthermochemical processes [161793] Even though the route ofproduction depends on the raw material it can be summarized asthe breaking of the biomaterial to simple sugars that furtherfermented using alcohol producing microorganisms The producedethanol later separated and concentrated through downstreamprocesses (Fig 4)

Facing the conflict of global energy and food demand therehave been increasing interest and worldwide studies in producingbioethanol from alternative sources like microalgae rather thanfeedstock that has minor impact in the daily life [161793]

Bioethanol from microalgae can be produced through thefermentation of the microalgal biomass or directly through cellularreactions [9495]

When considering ethanol production via fermentation the keyis the accumulation of starch which is a potential substrate thatcan reach half of the microalgas cellular dry biomass Microalgalstarch can be extracted by mechanical or enzymatic means andfurther separated by downstream processes incorporating wateror an organic solvent This starch will be hydrolyzed to glucose tobe used in ethanol fermentation [9697] Production mainly differsfrom other crop raw materials in the first steps of the processbecause microalgae will need special concentration harvestingand mechanical disruption systems related with their cellularphysiology and culturing [98]

Microalgae can also excrete ethanol directly through the cellwalls by means of intracellular processes under dark becauseillumination prevents the formation of ethanol except for minoramounts This process which is reported in some microalgae likeChlorococcum littorale [99] Chlamydomonas reinhardtii [8384]Chlamydomonas moewusii [100] Chlorella vulgaris [101] Oscilla-toria limnetica [102] Oscillatoria limosa [99] Gleocapsa alpicola[103] Spirulina platensis [68] Cyanoteche sp [99] covers theanaerobic metabolism in algae where the assimilation and forma-tion of hydrogen carbon dioxide formate acetate ethanol lactateglycerol and butannediol take place [1783] Degradation of intracel-lular starch which is the main endogenous carbon source storedduring aerobic phototrophic metabolism to pyruvate is accomplishedby the EmbdenndashMeyerhofndashParnas and pentose phosphate pathwaysusing pyruvate decarboxylase and alcohol dehydrogenase enzymes[99102] As stated by Gfeller and Gibbs [83] the lack of ethanolproduction by the microalgae cells during illumination is related withthe absence of available reduced pyridine nucleotides with theassumption of active acetaldehyde and alcohol dehydrogenases Twopossible conversion routes for acetyl-CoA to acetate and ethanol canbe followed In the former route half of the acetyl-CoA is converted toacetate by a deacylase while the rest is reduced to ethanol withacetaldehyde as intermediate In the latter route acetyl-CoA is reducedto acetaldehyde that undergoes a dismutation sequence until theformation of acetate and ethanol [8384]

Enhancing direct microalgal bioethanol production by geneticmanipulations is also under consideration Genes from the ethanolproducing bacterium Zymomonas mobilis was transfered intomicroalgae Synechococcus sp aiming to give the ability to utilizethe fixed carbon for direct ethanol excretion to the culture volumethrough the cell walls [93104]

The novelty of the process lies in the separation of producedbioethanol from the culture medium This process eliminates theharvesting step that decreases the energy costs and water usageassociated with the separation processes required for algae har-vesting and fuel extraction [94105]

Besides bioethanol being the main product the remainingmicroalgal biomass may be used to produce biomethane again

Table 4Microalgal hydrogen production

Microalgae Cultivation Process PBR type Culture medium Hydrogen productionprocedure

Time H2 production Refs

Anabaena variabilis (CCAP 14034B)

Continuousndashphotoautotrophic

Lab Stirred (300 mL) Nitrogen free Allen-Arnon

Nitrogen free Allen-Arnon medium

Under vacuum for 15 min Increased light intensity for

5 h at the 6th day ofcultivation

35 days 12ndash14 mL gminus1DW hminus1 [164]

Anabaena variabilis (ATCC 29413) Continuousndashphotoautotrophic

Lab Vial (14 mL) Allen-Arnon(containing Na2MoO4 orNa3VO4 or neither)

Under argon flushing 80ndash100 h

Up to 5 nmol hminus1 mg Chlaminus1 at pH levels of 7ndash9 with Na3VO4 added cultures

[165]

Anabaena sp PCC 7120 (3hydrogenase mutants from PCC7120)

Batchndashphotoautotrophic Lab Sealed polystyrenecuvettes (1 cm light path47 mL capacity)

BG 11 Nitrogen free BG 11 medium Under anaerobic conditions Various light intensities

32ndash40 h Up to 08ndash1 mmol per cuvette (47 mL) [63]

Anabaena sp PCC 7120 and itsmutant AMC 414

Continuousndashphotoautotrophic

Outdoor Tubular-coiled (435 L) BG 11 Nitrogen free BG 11 medium Under argon atmosphere Nitrogen free BG 11 medium Under anaerobic conditions Increased light intensity

7 days 149 mL hminus1Lminus1PBR (373 mL total) with themutant

[166]

Anabaena variabilis (ATCC 29413) Batchndashphotoautotrophic Lab Panel (500 mL capacity) BG 11 50 h Up to 40ndash50 mL [167]

Chlamydomonas reinhardtii(CC124)

BatchndashphotomixotrophicSynchronous andunsynchronous growth

Lab Stirred glass bottles(12L)

TAP TAP-S medium (transferred bycentrifugation)

140 h 102 mL (with 4 h synchronizedcultures)

86 mL (with unsynchronized cultures)

[168]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotomixotrophic Lab Stirred glass bottles(500 mL)

TAP TAP-S medium transfer bycentrifugation

TAP-S medium inoculationby TAP culture (10inoculation)

175 mL Lminus1 (with centrifuged cultures under20ndash40 mE mminus2sminus1 average light intensity)

[87]

Chlamydomonas reinhardtii(CC124)

Continuousndashphotomixotrophic

Lab Stirred glass bottles(1050 mL)

TAP-S (90 mmol sulfateadded)

TAP-S medium two stagechemostat with aerobicstage and anaerobic stage

TAP-S medium TAP medium with limiting

sulfate (10ndash20 mM) Anaerobic conditions Sulfur free medium Anaerobic

4000 h Up to 058 mL hminus1Lminus1PBR [169]

Chlamydomonas reinhardtii (Dang137C mt+ and a nonmotilemutant CC 1036 pf18 mt+)

Batchndashphotomixotrophic-immobilized

Lab Panel (160 mL) TAP (046 mM sulfatereplete)

23 days 45 mL dayminus1 (380 mL total) [170]

Chlamydomonas reinhardtii (Dang137C mt+)

Batch-photoautotrophicmixotrophic andheterotrophic

Lab Flat glass bottles PBR(15 L volume)

HS (CO2 bubbling) TAPwith or without CO2

bubbling

60ndash80 h 11704 mmol Lminus1 (sim28 mL (hL)minus1) inphotoautotrophic cultures

45716 mmol Lminus1 (sim40 mL (hL)minus1) inphotoheterotrophic cultures

09708 mmol Lminus1 (sim69 mL (hL)minus1)inphotomixotrophic cultures

[171]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotoautotrophic Lab Flat glass bottles PBR(15 L)

High salt HS sulfur free medium Argon purging during the

first 24 h of deprivation TAP-S medium Various dilutions Anaerobic conditions

100 h 7173 mL Lminus1 (175 mE mminus2sminus1 lightintensity pH 77)

5272 mL Lminus1 (420 mE mminus2sminus1 lightintensity pH 74)

[172]

Chlamydomonas reinhardtii(CC124)

Semi continuousndashphotomixotrophic

Lab Stirred tank (25 L) TAP 127 days 1108 mL [173]

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic-immobilized

Lab Vials (75 mL) TAP TA-S-P (no sulfate nophosphate) medium

Alginate entrapped

160ndash180 h

0307002 mol mminus2 (125 mmol mgminus1 Chl hminus1) [174]

Batchndashphotomixotrophic Lab Glass bottles (325 mL) TAP 192 h 395 mmol106 cellsminus1 hminus1 with TAP-S [90]

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ndash264250

harvested cells flushed withor without argon

Anaerobic conditions TAP-S or TAP-N DCMU mixed ethanol

addition Dark anaerobic

fermentation

Chlamydomonas reinhardtii(CC124)

34 mmol106 cellsminus1 hminus1 with TAP-N

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Stirred tank (1 255 L) TAP-S TAP-S medium transfer bycentrifugation

Various mixing time Various light energy Scale-up

192 h Max with 122 kJ sminus1 mminus3 light energy and25 min mixing time

[202]

1 L PBR 1537005 mL Lminus1 hminus1

25 L PBR 1327005 mL Lminus1 hminus1

5 L PBR 1027005 mL Lminus1 hminus1

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Tubular (110 L) TAP-S TAP-S medium transfer bycentrifugation

Modified with silicananoparticle to enhancescattering

48 h 3121571789 mL (06 mL Lminus1 hminus1) [203]

Chlorella pyrenoidosa C-101 Batchndashphotoautotrophic Lab Bubble column (650 mL) Modified Bristol Nitrogen flushing under dark forldquo420rdquo h

60ndash65 h 6910minus2 m3 kgminus1 cell [65]

Chlorella vulgaris MSU 01 Batchndashphotomixotrophic Lab Stirred (500 mL) Modified BG11 and MJ Anaerobic conditions Corn stalk as carbon source

in the medium

6ndash7 days 26 mL [175]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Dark incubation Anaerobic nitrogen

atmosphere Addition of specific effectors

(DCMU DCCD DBMIBand CCCP)

Continuous illuminationafterwards

8 h 0339 mL hminus1 Lminus1 (144 mL) based on1106 cells mLminus1 at 15 μM CCCP addedculture after 8 h of illumination

[66]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Sulfur deprive medium Incubation under dark Anaerobic conditions Continuous illumination

afterwards

50 h 11720 nL hminus1 (with seawater-S medium) [67]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Torus (15 L) Defined mineral Dark incubation Anaerobic nitrogen

atmosphere 15 μM CCCP addition Continuous illumination

afterwards

4ndash6 days 720 mL hminus1 (2366770 mL) [176]

Platymonas helgolandica vartsingtaoensis

Batchndashphotoautotrophic Lab Jars (130 mL) F2 Anaerobic Illuminated -S medium Dark CCCPDCMU or both

added medium

25 h 0002 mmol Lminus1 withndashS medium 0160 mmol Lminus1 with CCCP medium 0014 mmol Lminus1 with DCMU medium 0290 mmol Lminus1 with CCCP

+DCMU medium

[89]

Spirulina platensis (NIES-46) Batchndashphotoautotrophic Lab Erlenmeyer flasks(60 mL)

SOT Nitrogen free medium Under dark

20 h 2 mmol mgDWminus1 [68]

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Table

4(con

tinu

ed)

Micro

alga

eCu

ltivation

Pro

cess

PBRtype

Culture

med

ium

Hyd

roge

npro

duction

pro

cedure

Time

H2pro

duction

Refs

Anae

robicco

nditions

Syne

chocystissp

PCC68

03an

dits

mutantNDH-1

complex

defi

cien

tM55

Batch

ndashphotoa

utotrop

hicndash

encapsu

lated

Lab

Vials

(2mL)

BG

11

Nitroge

natmosphere

Under

cycled

lightan

ddark

exposure

5day

s0005

ndash004

5mM

[177

]

Tetraspo

rasp

CU25

51Batch

ndashphotom

ixotrophic

Lab

Vials

TAP(w

itho

rwithou

t05mM

β-mercaptoethan

olfor

24h)

Su

lfuran

dnitroge

ndep

rive

dmed

ium

Argon

flush

edan

aerobic

atmosphere

424

h173ndash61

7mm

olmgminus

1Chlahminus1

[178

]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264252

through anaerobic digestion for electricity generation The carbondioxide and discharged water formed as by-products of thefermentation can be recycled for the microalgae cultivation tofulfill the biorefinery concept [94105]

24 Biomethane

Today agricultural plants or by-products are conventionalsources for renewable biogas production which is mainly amixture of methane (55ndash75) and carbon dioxide (25ndash45) byanaerobic digestion Biomethane from the biogas can be used as afuel for transportation and electricity generation or for heatingpurposes especially in the rural areas [16106107]

Microalgae with their dominancy over crop plants by means ofproductivity per hectare triggered the attention for the production ofbiogas The solar energy converted and stored by the microalgae cellsthrough photosynthesis can be transformed into energy through theanaerobic digestion to produce methane [106108]

Microalgal biomass having high cellular lipid starch andprotein low cellulose and on the other hand the absence of ligningives a reliable and effective anaerobic digestion These specifica-tions make microalgae a good alternative for effective biomethaneproduction compared to the other crop plants [16107108]

Microalgal biomass can be processed anaerobically step by stepwith specialized groups of bacteria [109]

Hydrolyzation of biopolymers to monosaccharides by hydro-lytic bacteria

Fermentation of the monosaccharides to carboxylic acids andalcohols by fermentative bacteria

Conversion of the acids and alcohols to acetate hydrogen andcarbon dioxide by acetogenic bacteria

Conversion of the end products of acetogenic reactions tomethane and carbon dioxide by methanogenic bacteria

Microalgal biomass remaining after the anaerobic digestion canbe further processed to make fertilizers that can add an extra valueto the overall process Also the carbon dioxide portion of theproduced biogas can be recycled again to cultivate the neededmicroalgal biomass for processing [107110ndash112]

A predicted model of microalgae biomass for digestion toproduce electrical and thermal energy discussed the economicprofitability related with technical aspects of the productionsystem The results showed that the microalgae productivityharvesting concentration and usage of high rate anaerobic diges-ters are the key factors for the economic energy production [113]

A life cycle perspective study using a stochastic model indi-cated that when compared with the conventional crops likeswitch grass canola and corn the environmental impact ofmicroalgal biomass production is higher with respect to energydemand greenhouse gas emissions and water use regardless ofcultivation location Only in overall land use and eutrophicationpotential microalgae present favorable results [114] This mayseem to be a disadvantage to produce biomethane from microalgalbiomass but the studies also supported that the integratedprocesses using proper photobioreactors combining microalgaecultivation and waste water treatment systems for biomethaneproduction will help to reduce the environmental impacts result-ing in a competitive and effective production [11416115]

25 Integrated processes

Relations between parameters and the target products (bio-mass lipid hydrogen ethanol) are important in the selection ofthe microalgae for efficient biofuel production As can be followedfrom the tables summarizing the microalgal biofuel productions

Sugars

- Sugarcane juice

- Molasses

- Sugar beet

Starch

- Corn

- Oats

- Wheat

- Sago Palm

- Cassava

- Banana wastes

- Rye

- Barley

- Triticale

- Sorghum

- Algal biomass

Lignocellulosic materials

- Crop residues

- Cellulose wastes

- Hardwood

- Harbaceous biomass

- Softwood

- Municipal solid wastes

Fermentation

- Saccharomyces cerevisiae

- Schizosaccharomyces pombe

- Zymomonas mobilis

- Saccharomyces bayanus

- Pichia stipitis

- Candida shehatae

- Pachysolen tannophilus

- Mucor indicus

- Chalara parvispora

- T thermosaccharolyticum

- T Ethanolicus

- B Stearothermophilus

- C thermohydrosulfuricum

- C thermocellum

- Milling

- Grinding

- ShredingBreaking hemicellulose

chains

- Physical

- Chemical

- Physicochemical

- Biological

Hydrolization -Detoxification

-Neutralization

Sugars

- Hexoses

- Pentoses

Separation and

Concentration

- Distillation

- Rectification

- Dehydration

ETHANOL

Fig 4 Ethanol production from biomass productionSource Adapted from Refs [9398201]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 253

studies focus on the separation of production processes into twomain steps growth mediated and product mediated When con-sidering direct biofuel production the main approach is product

mediated for higher lipid hydrogen or ethanol production Whenconsidering biofuel production integrated with other microorgan-isms (Table 5) the main approach is growth mediated for higher

Table 5Integrated biofuel processes working with microalgae

Microalgae System Product Ref

Chlamydomonas reinhardtii (UTEX 90) Enzymatic treatment of algal biomass and conversion to ethanol by Saccharomyces cerevisiae Ethanol [179]Chlamydomonas reinhardtii (UTEX 90) Hydrothermal acid treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [180]Chlorella vulgaris (IAM C-534) Enzymatic treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [181]Synechococcus leopoliensis (IAMM 6) Fermentation of acid treated saccharified algal biomass by yeast Saccharomyces sake (IFO 2347) Ethanol [97]Chlamydomonas reinhardtii Chlorella vulgaris (macroalgae Undaria pinnatifida) Enzymatic treatment of pre-acid hydrolyzed algal biomass fermentation by 4 different strains of Escherichia coli Ethanol [182]Schizocytrium sp Fermentation of hydrothermal treated algal biomass by E coli KO11 Ethanol [183]Microcystis aeruginosa and Anabaena variabilis Hydrolysis and fermentation of Super Critical fluid pretreated algal biomass by Saccharomyces cerevisiae Ethanol [204]Scenedesmus obliquus Fermentation of algal biomass hydrolysate by Kluyveromyces marxianus IGC 2671 Saccharomyces carlsbergensis

ATCC6269 and Saccharomyces bayanusEthanol [205]

Anabaena sp PCC7120 Fermentation of hydrogen produced residual algal biomass by Enterobacter aerogenes Hydrogen [184]Arthrospira (Spirulina) platensis Nannochloropsis sp and Dunaliella tertilecta Anaerobic fermentation of thermal pretreated algal biomass by immobilized Clostridium acetobutylicum Hydrogen acetone

ethanol butanol[206]

Chlorella vulgaris ESP6 Dark fermentation of acid or alkalineenzyme pretreated algal biomass hydrolysate by Clostridium butyricumCGS5

Hydrogen [207]

Chlorella sp Simultaneous hydrolysis and fermentation of algal biomass by sewage sludge consortia Hydrogen [208]Thalassiosira weissflogii Dark fermentation of algal biomass with the thermophilic bacterium Thermotoga neapolitana Hydrogen [209]Chlamydomonas reinhardtii (IAM C-238) Chlorella pyrenoidosa (IAM C-212) andDunaliella tertiolecta (ATCC 30909)

Fermentation of algal biomass by Lactobacillus amylovorous (ATCC 33620) and Rhodobacter sphaeroides RV Hydrogen [185]

Chlamydomonas reinhardtii (IAM C-238) and Dunaliella tertiolecta (ATCC 30909) Fermentation of algal biomass by Lactobacillus amylovorous and Rhodobium marinum (A-501) mixed culture Hydrogen [186]Chlamydomonas (MGA 161) Fermentation of algal biomass by Rhodovulum sulfidophilum (W-1S) Hydrogen [85]Chlamydomonas reinhardtii (C238) Mixed cultivation of Chlamydomonas reinhardtii (C238) with Rhodospirillum rubrum (NCIB 8255) Hydrogen [187]Scnedesmus sp Fermentation of algal biomass by anaerobic digested sludge Hydrogen [188]Arthrospira maxima Anaerobic digestion of algal biomass by sewage sludge consortia Methane [210]Phaeodactylum tricornutum Anaerobic digestion of algal biomass by potato factory origin anaerobic granular sludge Methane [211]Scenedesmus sp Anaerobic digestion of high pressure thermal pretreated raw and residue (from lipid extraction) algal biomass

and by anaerobic digestor sludgeMethane [212]

Scenedesmus sp Anaerobic digestion of ultrasound and thermal pretreated raw algal biomass by sugar factory origin anaerobicgranular sludge

Methane [213]

Scenedesmus sp Anaerobic digestion of mild thermal pretreated raw algal biomass by sugar factory origin anaerobic granularsludge

Methane [214]

Spirulina platensis Anabaena variabilis and Chlorella sp Processing of algal biomass by an integrated system of methanogenic culture and Rhodobacter capsulatus Methane and hydrogen [189]Spirulina platensis (UTEX 1926) Rhodotorula glutinis (2541) Mixed cultivation of microalgae and yeast using waste water Lipid (biodiesel) [190]Spirulina platensis Using excess CO2 from the ethanol fermentation by Saccharomyces cerevisiae Lipid (biodiesel) [119]Botryococcus braunii (two strains BB763 and BB764) Chlorella vulgaris Chlorellapyrenoidosa

Biodiesel production catalyzed by immobilized Penicillium expansum lipase and Candida antarctica lipase B(Novozym 435)

Lipid (biodiesel) [191]

Chlorella vulgaris (21111B) Anaerobic digestion of algal biomass by sewage sludge origin methanogenic culture Methane [112]Chlorella sp and Scenedesmus Anaerobic digestion of algal biomass by sewage sludge culture Methane [106]Chlorella sp Anaerobic digestion of algal biomass by sludge culture Methane [192]Arthrospira platensis Chlamydomonas reinhardtii Chlorella kessleri Dunaliellasalina Euglena gracilis and Scenedesmus obliquus

Anaerobic digestion of algal biomass by sewage sludge culture Methane [107]

Spirulina maxima Anaerobic digestion of algal biomass by sewage sludge culture Methane [193]Chlorella sp and Scenedesmus Anaerobic codigestion of algal biomass with waste paper by methanogenic culture Methane [194]Tetraselmis Anaerobic digestion of algal biomass by methanogenic culture Methane [195]Chlorococcum sp Anaerobic treatment of distillery waste with algal biomass by acidogenicmethanogenic culture Methane [196]Phaeodactylum tricornutum (CCAP10551) Anaerobic digestion of algal biomass by granular seed sludge from digester treating potato processing waste

water dominated by Methanosaeta sp and Methanosarcina spMethane [197]

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biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

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technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

[1] EIA (US Energy Information Administration) International Energy Outlook2010 Washington DC 20585 US 2010 langwwweiagovoiafieoindexhtmlrang

[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264262

[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 10: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

Table 4Microalgal hydrogen production

Microalgae Cultivation Process PBR type Culture medium Hydrogen productionprocedure

Time H2 production Refs

Anabaena variabilis (CCAP 14034B)

Continuousndashphotoautotrophic

Lab Stirred (300 mL) Nitrogen free Allen-Arnon

Nitrogen free Allen-Arnon medium

Under vacuum for 15 min Increased light intensity for

5 h at the 6th day ofcultivation

35 days 12ndash14 mL gminus1DW hminus1 [164]

Anabaena variabilis (ATCC 29413) Continuousndashphotoautotrophic

Lab Vial (14 mL) Allen-Arnon(containing Na2MoO4 orNa3VO4 or neither)

Under argon flushing 80ndash100 h

Up to 5 nmol hminus1 mg Chlaminus1 at pH levels of 7ndash9 with Na3VO4 added cultures

[165]

Anabaena sp PCC 7120 (3hydrogenase mutants from PCC7120)

Batchndashphotoautotrophic Lab Sealed polystyrenecuvettes (1 cm light path47 mL capacity)

BG 11 Nitrogen free BG 11 medium Under anaerobic conditions Various light intensities

32ndash40 h Up to 08ndash1 mmol per cuvette (47 mL) [63]

Anabaena sp PCC 7120 and itsmutant AMC 414

Continuousndashphotoautotrophic

Outdoor Tubular-coiled (435 L) BG 11 Nitrogen free BG 11 medium Under argon atmosphere Nitrogen free BG 11 medium Under anaerobic conditions Increased light intensity

7 days 149 mL hminus1Lminus1PBR (373 mL total) with themutant

[166]

Anabaena variabilis (ATCC 29413) Batchndashphotoautotrophic Lab Panel (500 mL capacity) BG 11 50 h Up to 40ndash50 mL [167]

Chlamydomonas reinhardtii(CC124)

BatchndashphotomixotrophicSynchronous andunsynchronous growth

Lab Stirred glass bottles(12L)

TAP TAP-S medium (transferred bycentrifugation)

140 h 102 mL (with 4 h synchronizedcultures)

86 mL (with unsynchronized cultures)

[168]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotomixotrophic Lab Stirred glass bottles(500 mL)

TAP TAP-S medium transfer bycentrifugation

TAP-S medium inoculationby TAP culture (10inoculation)

175 mL Lminus1 (with centrifuged cultures under20ndash40 mE mminus2sminus1 average light intensity)

[87]

Chlamydomonas reinhardtii(CC124)

Continuousndashphotomixotrophic

Lab Stirred glass bottles(1050 mL)

TAP-S (90 mmol sulfateadded)

TAP-S medium two stagechemostat with aerobicstage and anaerobic stage

TAP-S medium TAP medium with limiting

sulfate (10ndash20 mM) Anaerobic conditions Sulfur free medium Anaerobic

4000 h Up to 058 mL hminus1Lminus1PBR [169]

Chlamydomonas reinhardtii (Dang137C mt+ and a nonmotilemutant CC 1036 pf18 mt+)

Batchndashphotomixotrophic-immobilized

Lab Panel (160 mL) TAP (046 mM sulfatereplete)

23 days 45 mL dayminus1 (380 mL total) [170]

Chlamydomonas reinhardtii (Dang137C mt+)

Batch-photoautotrophicmixotrophic andheterotrophic

Lab Flat glass bottles PBR(15 L volume)

HS (CO2 bubbling) TAPwith or without CO2

bubbling

60ndash80 h 11704 mmol Lminus1 (sim28 mL (hL)minus1) inphotoautotrophic cultures

45716 mmol Lminus1 (sim40 mL (hL)minus1) inphotoheterotrophic cultures

09708 mmol Lminus1 (sim69 mL (hL)minus1)inphotomixotrophic cultures

[171]

Chlamydomonas reinhardtii (Dang137C mt+)

Batchndashphotoautotrophic Lab Flat glass bottles PBR(15 L)

High salt HS sulfur free medium Argon purging during the

first 24 h of deprivation TAP-S medium Various dilutions Anaerobic conditions

100 h 7173 mL Lminus1 (175 mE mminus2sminus1 lightintensity pH 77)

5272 mL Lminus1 (420 mE mminus2sminus1 lightintensity pH 74)

[172]

Chlamydomonas reinhardtii(CC124)

Semi continuousndashphotomixotrophic

Lab Stirred tank (25 L) TAP 127 days 1108 mL [173]

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic-immobilized

Lab Vials (75 mL) TAP TA-S-P (no sulfate nophosphate) medium

Alginate entrapped

160ndash180 h

0307002 mol mminus2 (125 mmol mgminus1 Chl hminus1) [174]

Batchndashphotomixotrophic Lab Glass bottles (325 mL) TAP 192 h 395 mmol106 cellsminus1 hminus1 with TAP-S [90]

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harvested cells flushed withor without argon

Anaerobic conditions TAP-S or TAP-N DCMU mixed ethanol

addition Dark anaerobic

fermentation

Chlamydomonas reinhardtii(CC124)

34 mmol106 cellsminus1 hminus1 with TAP-N

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Stirred tank (1 255 L) TAP-S TAP-S medium transfer bycentrifugation

Various mixing time Various light energy Scale-up

192 h Max with 122 kJ sminus1 mminus3 light energy and25 min mixing time

[202]

1 L PBR 1537005 mL Lminus1 hminus1

25 L PBR 1327005 mL Lminus1 hminus1

5 L PBR 1027005 mL Lminus1 hminus1

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Tubular (110 L) TAP-S TAP-S medium transfer bycentrifugation

Modified with silicananoparticle to enhancescattering

48 h 3121571789 mL (06 mL Lminus1 hminus1) [203]

Chlorella pyrenoidosa C-101 Batchndashphotoautotrophic Lab Bubble column (650 mL) Modified Bristol Nitrogen flushing under dark forldquo420rdquo h

60ndash65 h 6910minus2 m3 kgminus1 cell [65]

Chlorella vulgaris MSU 01 Batchndashphotomixotrophic Lab Stirred (500 mL) Modified BG11 and MJ Anaerobic conditions Corn stalk as carbon source

in the medium

6ndash7 days 26 mL [175]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Dark incubation Anaerobic nitrogen

atmosphere Addition of specific effectors

(DCMU DCCD DBMIBand CCCP)

Continuous illuminationafterwards

8 h 0339 mL hminus1 Lminus1 (144 mL) based on1106 cells mLminus1 at 15 μM CCCP addedculture after 8 h of illumination

[66]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Sulfur deprive medium Incubation under dark Anaerobic conditions Continuous illumination

afterwards

50 h 11720 nL hminus1 (with seawater-S medium) [67]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Torus (15 L) Defined mineral Dark incubation Anaerobic nitrogen

atmosphere 15 μM CCCP addition Continuous illumination

afterwards

4ndash6 days 720 mL hminus1 (2366770 mL) [176]

Platymonas helgolandica vartsingtaoensis

Batchndashphotoautotrophic Lab Jars (130 mL) F2 Anaerobic Illuminated -S medium Dark CCCPDCMU or both

added medium

25 h 0002 mmol Lminus1 withndashS medium 0160 mmol Lminus1 with CCCP medium 0014 mmol Lminus1 with DCMU medium 0290 mmol Lminus1 with CCCP

+DCMU medium

[89]

Spirulina platensis (NIES-46) Batchndashphotoautotrophic Lab Erlenmeyer flasks(60 mL)

SOT Nitrogen free medium Under dark

20 h 2 mmol mgDWminus1 [68]

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Table

4(con

tinu

ed)

Micro

alga

eCu

ltivation

Pro

cess

PBRtype

Culture

med

ium

Hyd

roge

npro

duction

pro

cedure

Time

H2pro

duction

Refs

Anae

robicco

nditions

Syne

chocystissp

PCC68

03an

dits

mutantNDH-1

complex

defi

cien

tM55

Batch

ndashphotoa

utotrop

hicndash

encapsu

lated

Lab

Vials

(2mL)

BG

11

Nitroge

natmosphere

Under

cycled

lightan

ddark

exposure

5day

s0005

ndash004

5mM

[177

]

Tetraspo

rasp

CU25

51Batch

ndashphotom

ixotrophic

Lab

Vials

TAP(w

itho

rwithou

t05mM

β-mercaptoethan

olfor

24h)

Su

lfuran

dnitroge

ndep

rive

dmed

ium

Argon

flush

edan

aerobic

atmosphere

424

h173ndash61

7mm

olmgminus

1Chlahminus1

[178

]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264252

through anaerobic digestion for electricity generation The carbondioxide and discharged water formed as by-products of thefermentation can be recycled for the microalgae cultivation tofulfill the biorefinery concept [94105]

24 Biomethane

Today agricultural plants or by-products are conventionalsources for renewable biogas production which is mainly amixture of methane (55ndash75) and carbon dioxide (25ndash45) byanaerobic digestion Biomethane from the biogas can be used as afuel for transportation and electricity generation or for heatingpurposes especially in the rural areas [16106107]

Microalgae with their dominancy over crop plants by means ofproductivity per hectare triggered the attention for the production ofbiogas The solar energy converted and stored by the microalgae cellsthrough photosynthesis can be transformed into energy through theanaerobic digestion to produce methane [106108]

Microalgal biomass having high cellular lipid starch andprotein low cellulose and on the other hand the absence of ligningives a reliable and effective anaerobic digestion These specifica-tions make microalgae a good alternative for effective biomethaneproduction compared to the other crop plants [16107108]

Microalgal biomass can be processed anaerobically step by stepwith specialized groups of bacteria [109]

Hydrolyzation of biopolymers to monosaccharides by hydro-lytic bacteria

Fermentation of the monosaccharides to carboxylic acids andalcohols by fermentative bacteria

Conversion of the acids and alcohols to acetate hydrogen andcarbon dioxide by acetogenic bacteria

Conversion of the end products of acetogenic reactions tomethane and carbon dioxide by methanogenic bacteria

Microalgal biomass remaining after the anaerobic digestion canbe further processed to make fertilizers that can add an extra valueto the overall process Also the carbon dioxide portion of theproduced biogas can be recycled again to cultivate the neededmicroalgal biomass for processing [107110ndash112]

A predicted model of microalgae biomass for digestion toproduce electrical and thermal energy discussed the economicprofitability related with technical aspects of the productionsystem The results showed that the microalgae productivityharvesting concentration and usage of high rate anaerobic diges-ters are the key factors for the economic energy production [113]

A life cycle perspective study using a stochastic model indi-cated that when compared with the conventional crops likeswitch grass canola and corn the environmental impact ofmicroalgal biomass production is higher with respect to energydemand greenhouse gas emissions and water use regardless ofcultivation location Only in overall land use and eutrophicationpotential microalgae present favorable results [114] This mayseem to be a disadvantage to produce biomethane from microalgalbiomass but the studies also supported that the integratedprocesses using proper photobioreactors combining microalgaecultivation and waste water treatment systems for biomethaneproduction will help to reduce the environmental impacts result-ing in a competitive and effective production [11416115]

25 Integrated processes

Relations between parameters and the target products (bio-mass lipid hydrogen ethanol) are important in the selection ofthe microalgae for efficient biofuel production As can be followedfrom the tables summarizing the microalgal biofuel productions

Sugars

- Sugarcane juice

- Molasses

- Sugar beet

Starch

- Corn

- Oats

- Wheat

- Sago Palm

- Cassava

- Banana wastes

- Rye

- Barley

- Triticale

- Sorghum

- Algal biomass

Lignocellulosic materials

- Crop residues

- Cellulose wastes

- Hardwood

- Harbaceous biomass

- Softwood

- Municipal solid wastes

Fermentation

- Saccharomyces cerevisiae

- Schizosaccharomyces pombe

- Zymomonas mobilis

- Saccharomyces bayanus

- Pichia stipitis

- Candida shehatae

- Pachysolen tannophilus

- Mucor indicus

- Chalara parvispora

- T thermosaccharolyticum

- T Ethanolicus

- B Stearothermophilus

- C thermohydrosulfuricum

- C thermocellum

- Milling

- Grinding

- ShredingBreaking hemicellulose

chains

- Physical

- Chemical

- Physicochemical

- Biological

Hydrolization -Detoxification

-Neutralization

Sugars

- Hexoses

- Pentoses

Separation and

Concentration

- Distillation

- Rectification

- Dehydration

ETHANOL

Fig 4 Ethanol production from biomass productionSource Adapted from Refs [9398201]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 253

studies focus on the separation of production processes into twomain steps growth mediated and product mediated When con-sidering direct biofuel production the main approach is product

mediated for higher lipid hydrogen or ethanol production Whenconsidering biofuel production integrated with other microorgan-isms (Table 5) the main approach is growth mediated for higher

Table 5Integrated biofuel processes working with microalgae

Microalgae System Product Ref

Chlamydomonas reinhardtii (UTEX 90) Enzymatic treatment of algal biomass and conversion to ethanol by Saccharomyces cerevisiae Ethanol [179]Chlamydomonas reinhardtii (UTEX 90) Hydrothermal acid treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [180]Chlorella vulgaris (IAM C-534) Enzymatic treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [181]Synechococcus leopoliensis (IAMM 6) Fermentation of acid treated saccharified algal biomass by yeast Saccharomyces sake (IFO 2347) Ethanol [97]Chlamydomonas reinhardtii Chlorella vulgaris (macroalgae Undaria pinnatifida) Enzymatic treatment of pre-acid hydrolyzed algal biomass fermentation by 4 different strains of Escherichia coli Ethanol [182]Schizocytrium sp Fermentation of hydrothermal treated algal biomass by E coli KO11 Ethanol [183]Microcystis aeruginosa and Anabaena variabilis Hydrolysis and fermentation of Super Critical fluid pretreated algal biomass by Saccharomyces cerevisiae Ethanol [204]Scenedesmus obliquus Fermentation of algal biomass hydrolysate by Kluyveromyces marxianus IGC 2671 Saccharomyces carlsbergensis

ATCC6269 and Saccharomyces bayanusEthanol [205]

Anabaena sp PCC7120 Fermentation of hydrogen produced residual algal biomass by Enterobacter aerogenes Hydrogen [184]Arthrospira (Spirulina) platensis Nannochloropsis sp and Dunaliella tertilecta Anaerobic fermentation of thermal pretreated algal biomass by immobilized Clostridium acetobutylicum Hydrogen acetone

ethanol butanol[206]

Chlorella vulgaris ESP6 Dark fermentation of acid or alkalineenzyme pretreated algal biomass hydrolysate by Clostridium butyricumCGS5

Hydrogen [207]

Chlorella sp Simultaneous hydrolysis and fermentation of algal biomass by sewage sludge consortia Hydrogen [208]Thalassiosira weissflogii Dark fermentation of algal biomass with the thermophilic bacterium Thermotoga neapolitana Hydrogen [209]Chlamydomonas reinhardtii (IAM C-238) Chlorella pyrenoidosa (IAM C-212) andDunaliella tertiolecta (ATCC 30909)

Fermentation of algal biomass by Lactobacillus amylovorous (ATCC 33620) and Rhodobacter sphaeroides RV Hydrogen [185]

Chlamydomonas reinhardtii (IAM C-238) and Dunaliella tertiolecta (ATCC 30909) Fermentation of algal biomass by Lactobacillus amylovorous and Rhodobium marinum (A-501) mixed culture Hydrogen [186]Chlamydomonas (MGA 161) Fermentation of algal biomass by Rhodovulum sulfidophilum (W-1S) Hydrogen [85]Chlamydomonas reinhardtii (C238) Mixed cultivation of Chlamydomonas reinhardtii (C238) with Rhodospirillum rubrum (NCIB 8255) Hydrogen [187]Scnedesmus sp Fermentation of algal biomass by anaerobic digested sludge Hydrogen [188]Arthrospira maxima Anaerobic digestion of algal biomass by sewage sludge consortia Methane [210]Phaeodactylum tricornutum Anaerobic digestion of algal biomass by potato factory origin anaerobic granular sludge Methane [211]Scenedesmus sp Anaerobic digestion of high pressure thermal pretreated raw and residue (from lipid extraction) algal biomass

and by anaerobic digestor sludgeMethane [212]

Scenedesmus sp Anaerobic digestion of ultrasound and thermal pretreated raw algal biomass by sugar factory origin anaerobicgranular sludge

Methane [213]

Scenedesmus sp Anaerobic digestion of mild thermal pretreated raw algal biomass by sugar factory origin anaerobic granularsludge

Methane [214]

Spirulina platensis Anabaena variabilis and Chlorella sp Processing of algal biomass by an integrated system of methanogenic culture and Rhodobacter capsulatus Methane and hydrogen [189]Spirulina platensis (UTEX 1926) Rhodotorula glutinis (2541) Mixed cultivation of microalgae and yeast using waste water Lipid (biodiesel) [190]Spirulina platensis Using excess CO2 from the ethanol fermentation by Saccharomyces cerevisiae Lipid (biodiesel) [119]Botryococcus braunii (two strains BB763 and BB764) Chlorella vulgaris Chlorellapyrenoidosa

Biodiesel production catalyzed by immobilized Penicillium expansum lipase and Candida antarctica lipase B(Novozym 435)

Lipid (biodiesel) [191]

Chlorella vulgaris (21111B) Anaerobic digestion of algal biomass by sewage sludge origin methanogenic culture Methane [112]Chlorella sp and Scenedesmus Anaerobic digestion of algal biomass by sewage sludge culture Methane [106]Chlorella sp Anaerobic digestion of algal biomass by sludge culture Methane [192]Arthrospira platensis Chlamydomonas reinhardtii Chlorella kessleri Dunaliellasalina Euglena gracilis and Scenedesmus obliquus

Anaerobic digestion of algal biomass by sewage sludge culture Methane [107]

Spirulina maxima Anaerobic digestion of algal biomass by sewage sludge culture Methane [193]Chlorella sp and Scenedesmus Anaerobic codigestion of algal biomass with waste paper by methanogenic culture Methane [194]Tetraselmis Anaerobic digestion of algal biomass by methanogenic culture Methane [195]Chlorococcum sp Anaerobic treatment of distillery waste with algal biomass by acidogenicmethanogenic culture Methane [196]Phaeodactylum tricornutum (CCAP10551) Anaerobic digestion of algal biomass by granular seed sludge from digester treating potato processing waste

water dominated by Methanosaeta sp and Methanosarcina spMethane [197]

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 255

biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264256

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

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Renew

ableand

SustainableEnergy

Review

s26

(2013)241

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 259

technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

[1] EIA (US Energy Information Administration) International Energy Outlook2010 Washington DC 20585 US 2010 langwwweiagovoiafieoindexhtmlrang

[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264262

[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 11: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

harvested cells flushed withor without argon

Anaerobic conditions TAP-S or TAP-N DCMU mixed ethanol

addition Dark anaerobic

fermentation

Chlamydomonas reinhardtii(CC124)

34 mmol106 cellsminus1 hminus1 with TAP-N

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Stirred tank (1 255 L) TAP-S TAP-S medium transfer bycentrifugation

Various mixing time Various light energy Scale-up

192 h Max with 122 kJ sminus1 mminus3 light energy and25 min mixing time

[202]

1 L PBR 1537005 mL Lminus1 hminus1

25 L PBR 1327005 mL Lminus1 hminus1

5 L PBR 1027005 mL Lminus1 hminus1

Chlamydomonas reinhardtii(CC124)

Batchndashphotomixotrophic Lab Tubular (110 L) TAP-S TAP-S medium transfer bycentrifugation

Modified with silicananoparticle to enhancescattering

48 h 3121571789 mL (06 mL Lminus1 hminus1) [203]

Chlorella pyrenoidosa C-101 Batchndashphotoautotrophic Lab Bubble column (650 mL) Modified Bristol Nitrogen flushing under dark forldquo420rdquo h

60ndash65 h 6910minus2 m3 kgminus1 cell [65]

Chlorella vulgaris MSU 01 Batchndashphotomixotrophic Lab Stirred (500 mL) Modified BG11 and MJ Anaerobic conditions Corn stalk as carbon source

in the medium

6ndash7 days 26 mL [175]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Dark incubation Anaerobic nitrogen

atmosphere Addition of specific effectors

(DCMU DCCD DBMIBand CCCP)

Continuous illuminationafterwards

8 h 0339 mL hminus1 Lminus1 (144 mL) based on1106 cells mLminus1 at 15 μM CCCP addedculture after 8 h of illumination

[66]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Serum bottle (295 mL) Sea water medium Sulfur deprive medium Incubation under dark Anaerobic conditions Continuous illumination

afterwards

50 h 11720 nL hminus1 (with seawater-S medium) [67]

Platymonas subcordiformis Batchndashphotoautotrophic Lab Torus (15 L) Defined mineral Dark incubation Anaerobic nitrogen

atmosphere 15 μM CCCP addition Continuous illumination

afterwards

4ndash6 days 720 mL hminus1 (2366770 mL) [176]

Platymonas helgolandica vartsingtaoensis

Batchndashphotoautotrophic Lab Jars (130 mL) F2 Anaerobic Illuminated -S medium Dark CCCPDCMU or both

added medium

25 h 0002 mmol Lminus1 withndashS medium 0160 mmol Lminus1 with CCCP medium 0014 mmol Lminus1 with DCMU medium 0290 mmol Lminus1 with CCCP

+DCMU medium

[89]

Spirulina platensis (NIES-46) Batchndashphotoautotrophic Lab Erlenmeyer flasks(60 mL)

SOT Nitrogen free medium Under dark

20 h 2 mmol mgDWminus1 [68]

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Table

4(con

tinu

ed)

Micro

alga

eCu

ltivation

Pro

cess

PBRtype

Culture

med

ium

Hyd

roge

npro

duction

pro

cedure

Time

H2pro

duction

Refs

Anae

robicco

nditions

Syne

chocystissp

PCC68

03an

dits

mutantNDH-1

complex

defi

cien

tM55

Batch

ndashphotoa

utotrop

hicndash

encapsu

lated

Lab

Vials

(2mL)

BG

11

Nitroge

natmosphere

Under

cycled

lightan

ddark

exposure

5day

s0005

ndash004

5mM

[177

]

Tetraspo

rasp

CU25

51Batch

ndashphotom

ixotrophic

Lab

Vials

TAP(w

itho

rwithou

t05mM

β-mercaptoethan

olfor

24h)

Su

lfuran

dnitroge

ndep

rive

dmed

ium

Argon

flush

edan

aerobic

atmosphere

424

h173ndash61

7mm

olmgminus

1Chlahminus1

[178

]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264252

through anaerobic digestion for electricity generation The carbondioxide and discharged water formed as by-products of thefermentation can be recycled for the microalgae cultivation tofulfill the biorefinery concept [94105]

24 Biomethane

Today agricultural plants or by-products are conventionalsources for renewable biogas production which is mainly amixture of methane (55ndash75) and carbon dioxide (25ndash45) byanaerobic digestion Biomethane from the biogas can be used as afuel for transportation and electricity generation or for heatingpurposes especially in the rural areas [16106107]

Microalgae with their dominancy over crop plants by means ofproductivity per hectare triggered the attention for the production ofbiogas The solar energy converted and stored by the microalgae cellsthrough photosynthesis can be transformed into energy through theanaerobic digestion to produce methane [106108]

Microalgal biomass having high cellular lipid starch andprotein low cellulose and on the other hand the absence of ligningives a reliable and effective anaerobic digestion These specifica-tions make microalgae a good alternative for effective biomethaneproduction compared to the other crop plants [16107108]

Microalgal biomass can be processed anaerobically step by stepwith specialized groups of bacteria [109]

Hydrolyzation of biopolymers to monosaccharides by hydro-lytic bacteria

Fermentation of the monosaccharides to carboxylic acids andalcohols by fermentative bacteria

Conversion of the acids and alcohols to acetate hydrogen andcarbon dioxide by acetogenic bacteria

Conversion of the end products of acetogenic reactions tomethane and carbon dioxide by methanogenic bacteria

Microalgal biomass remaining after the anaerobic digestion canbe further processed to make fertilizers that can add an extra valueto the overall process Also the carbon dioxide portion of theproduced biogas can be recycled again to cultivate the neededmicroalgal biomass for processing [107110ndash112]

A predicted model of microalgae biomass for digestion toproduce electrical and thermal energy discussed the economicprofitability related with technical aspects of the productionsystem The results showed that the microalgae productivityharvesting concentration and usage of high rate anaerobic diges-ters are the key factors for the economic energy production [113]

A life cycle perspective study using a stochastic model indi-cated that when compared with the conventional crops likeswitch grass canola and corn the environmental impact ofmicroalgal biomass production is higher with respect to energydemand greenhouse gas emissions and water use regardless ofcultivation location Only in overall land use and eutrophicationpotential microalgae present favorable results [114] This mayseem to be a disadvantage to produce biomethane from microalgalbiomass but the studies also supported that the integratedprocesses using proper photobioreactors combining microalgaecultivation and waste water treatment systems for biomethaneproduction will help to reduce the environmental impacts result-ing in a competitive and effective production [11416115]

25 Integrated processes

Relations between parameters and the target products (bio-mass lipid hydrogen ethanol) are important in the selection ofthe microalgae for efficient biofuel production As can be followedfrom the tables summarizing the microalgal biofuel productions

Sugars

- Sugarcane juice

- Molasses

- Sugar beet

Starch

- Corn

- Oats

- Wheat

- Sago Palm

- Cassava

- Banana wastes

- Rye

- Barley

- Triticale

- Sorghum

- Algal biomass

Lignocellulosic materials

- Crop residues

- Cellulose wastes

- Hardwood

- Harbaceous biomass

- Softwood

- Municipal solid wastes

Fermentation

- Saccharomyces cerevisiae

- Schizosaccharomyces pombe

- Zymomonas mobilis

- Saccharomyces bayanus

- Pichia stipitis

- Candida shehatae

- Pachysolen tannophilus

- Mucor indicus

- Chalara parvispora

- T thermosaccharolyticum

- T Ethanolicus

- B Stearothermophilus

- C thermohydrosulfuricum

- C thermocellum

- Milling

- Grinding

- ShredingBreaking hemicellulose

chains

- Physical

- Chemical

- Physicochemical

- Biological

Hydrolization -Detoxification

-Neutralization

Sugars

- Hexoses

- Pentoses

Separation and

Concentration

- Distillation

- Rectification

- Dehydration

ETHANOL

Fig 4 Ethanol production from biomass productionSource Adapted from Refs [9398201]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 253

studies focus on the separation of production processes into twomain steps growth mediated and product mediated When con-sidering direct biofuel production the main approach is product

mediated for higher lipid hydrogen or ethanol production Whenconsidering biofuel production integrated with other microorgan-isms (Table 5) the main approach is growth mediated for higher

Table 5Integrated biofuel processes working with microalgae

Microalgae System Product Ref

Chlamydomonas reinhardtii (UTEX 90) Enzymatic treatment of algal biomass and conversion to ethanol by Saccharomyces cerevisiae Ethanol [179]Chlamydomonas reinhardtii (UTEX 90) Hydrothermal acid treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [180]Chlorella vulgaris (IAM C-534) Enzymatic treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [181]Synechococcus leopoliensis (IAMM 6) Fermentation of acid treated saccharified algal biomass by yeast Saccharomyces sake (IFO 2347) Ethanol [97]Chlamydomonas reinhardtii Chlorella vulgaris (macroalgae Undaria pinnatifida) Enzymatic treatment of pre-acid hydrolyzed algal biomass fermentation by 4 different strains of Escherichia coli Ethanol [182]Schizocytrium sp Fermentation of hydrothermal treated algal biomass by E coli KO11 Ethanol [183]Microcystis aeruginosa and Anabaena variabilis Hydrolysis and fermentation of Super Critical fluid pretreated algal biomass by Saccharomyces cerevisiae Ethanol [204]Scenedesmus obliquus Fermentation of algal biomass hydrolysate by Kluyveromyces marxianus IGC 2671 Saccharomyces carlsbergensis

ATCC6269 and Saccharomyces bayanusEthanol [205]

Anabaena sp PCC7120 Fermentation of hydrogen produced residual algal biomass by Enterobacter aerogenes Hydrogen [184]Arthrospira (Spirulina) platensis Nannochloropsis sp and Dunaliella tertilecta Anaerobic fermentation of thermal pretreated algal biomass by immobilized Clostridium acetobutylicum Hydrogen acetone

ethanol butanol[206]

Chlorella vulgaris ESP6 Dark fermentation of acid or alkalineenzyme pretreated algal biomass hydrolysate by Clostridium butyricumCGS5

Hydrogen [207]

Chlorella sp Simultaneous hydrolysis and fermentation of algal biomass by sewage sludge consortia Hydrogen [208]Thalassiosira weissflogii Dark fermentation of algal biomass with the thermophilic bacterium Thermotoga neapolitana Hydrogen [209]Chlamydomonas reinhardtii (IAM C-238) Chlorella pyrenoidosa (IAM C-212) andDunaliella tertiolecta (ATCC 30909)

Fermentation of algal biomass by Lactobacillus amylovorous (ATCC 33620) and Rhodobacter sphaeroides RV Hydrogen [185]

Chlamydomonas reinhardtii (IAM C-238) and Dunaliella tertiolecta (ATCC 30909) Fermentation of algal biomass by Lactobacillus amylovorous and Rhodobium marinum (A-501) mixed culture Hydrogen [186]Chlamydomonas (MGA 161) Fermentation of algal biomass by Rhodovulum sulfidophilum (W-1S) Hydrogen [85]Chlamydomonas reinhardtii (C238) Mixed cultivation of Chlamydomonas reinhardtii (C238) with Rhodospirillum rubrum (NCIB 8255) Hydrogen [187]Scnedesmus sp Fermentation of algal biomass by anaerobic digested sludge Hydrogen [188]Arthrospira maxima Anaerobic digestion of algal biomass by sewage sludge consortia Methane [210]Phaeodactylum tricornutum Anaerobic digestion of algal biomass by potato factory origin anaerobic granular sludge Methane [211]Scenedesmus sp Anaerobic digestion of high pressure thermal pretreated raw and residue (from lipid extraction) algal biomass

and by anaerobic digestor sludgeMethane [212]

Scenedesmus sp Anaerobic digestion of ultrasound and thermal pretreated raw algal biomass by sugar factory origin anaerobicgranular sludge

Methane [213]

Scenedesmus sp Anaerobic digestion of mild thermal pretreated raw algal biomass by sugar factory origin anaerobic granularsludge

Methane [214]

Spirulina platensis Anabaena variabilis and Chlorella sp Processing of algal biomass by an integrated system of methanogenic culture and Rhodobacter capsulatus Methane and hydrogen [189]Spirulina platensis (UTEX 1926) Rhodotorula glutinis (2541) Mixed cultivation of microalgae and yeast using waste water Lipid (biodiesel) [190]Spirulina platensis Using excess CO2 from the ethanol fermentation by Saccharomyces cerevisiae Lipid (biodiesel) [119]Botryococcus braunii (two strains BB763 and BB764) Chlorella vulgaris Chlorellapyrenoidosa

Biodiesel production catalyzed by immobilized Penicillium expansum lipase and Candida antarctica lipase B(Novozym 435)

Lipid (biodiesel) [191]

Chlorella vulgaris (21111B) Anaerobic digestion of algal biomass by sewage sludge origin methanogenic culture Methane [112]Chlorella sp and Scenedesmus Anaerobic digestion of algal biomass by sewage sludge culture Methane [106]Chlorella sp Anaerobic digestion of algal biomass by sludge culture Methane [192]Arthrospira platensis Chlamydomonas reinhardtii Chlorella kessleri Dunaliellasalina Euglena gracilis and Scenedesmus obliquus

Anaerobic digestion of algal biomass by sewage sludge culture Methane [107]

Spirulina maxima Anaerobic digestion of algal biomass by sewage sludge culture Methane [193]Chlorella sp and Scenedesmus Anaerobic codigestion of algal biomass with waste paper by methanogenic culture Methane [194]Tetraselmis Anaerobic digestion of algal biomass by methanogenic culture Methane [195]Chlorococcum sp Anaerobic treatment of distillery waste with algal biomass by acidogenicmethanogenic culture Methane [196]Phaeodactylum tricornutum (CCAP10551) Anaerobic digestion of algal biomass by granular seed sludge from digester treating potato processing waste

water dominated by Methanosaeta sp and Methanosarcina spMethane [197]

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 255

biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264256

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

SSOncel

Renew

ableand

SustainableEnergy

Review

s26

(2013)241

ndash264258

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 259

technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

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[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264262

[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 12: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

Table

4(con

tinu

ed)

Micro

alga

eCu

ltivation

Pro

cess

PBRtype

Culture

med

ium

Hyd

roge

npro

duction

pro

cedure

Time

H2pro

duction

Refs

Anae

robicco

nditions

Syne

chocystissp

PCC68

03an

dits

mutantNDH-1

complex

defi

cien

tM55

Batch

ndashphotoa

utotrop

hicndash

encapsu

lated

Lab

Vials

(2mL)

BG

11

Nitroge

natmosphere

Under

cycled

lightan

ddark

exposure

5day

s0005

ndash004

5mM

[177

]

Tetraspo

rasp

CU25

51Batch

ndashphotom

ixotrophic

Lab

Vials

TAP(w

itho

rwithou

t05mM

β-mercaptoethan

olfor

24h)

Su

lfuran

dnitroge

ndep

rive

dmed

ium

Argon

flush

edan

aerobic

atmosphere

424

h173ndash61

7mm

olmgminus

1Chlahminus1

[178

]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264252

through anaerobic digestion for electricity generation The carbondioxide and discharged water formed as by-products of thefermentation can be recycled for the microalgae cultivation tofulfill the biorefinery concept [94105]

24 Biomethane

Today agricultural plants or by-products are conventionalsources for renewable biogas production which is mainly amixture of methane (55ndash75) and carbon dioxide (25ndash45) byanaerobic digestion Biomethane from the biogas can be used as afuel for transportation and electricity generation or for heatingpurposes especially in the rural areas [16106107]

Microalgae with their dominancy over crop plants by means ofproductivity per hectare triggered the attention for the production ofbiogas The solar energy converted and stored by the microalgae cellsthrough photosynthesis can be transformed into energy through theanaerobic digestion to produce methane [106108]

Microalgal biomass having high cellular lipid starch andprotein low cellulose and on the other hand the absence of ligningives a reliable and effective anaerobic digestion These specifica-tions make microalgae a good alternative for effective biomethaneproduction compared to the other crop plants [16107108]

Microalgal biomass can be processed anaerobically step by stepwith specialized groups of bacteria [109]

Hydrolyzation of biopolymers to monosaccharides by hydro-lytic bacteria

Fermentation of the monosaccharides to carboxylic acids andalcohols by fermentative bacteria

Conversion of the acids and alcohols to acetate hydrogen andcarbon dioxide by acetogenic bacteria

Conversion of the end products of acetogenic reactions tomethane and carbon dioxide by methanogenic bacteria

Microalgal biomass remaining after the anaerobic digestion canbe further processed to make fertilizers that can add an extra valueto the overall process Also the carbon dioxide portion of theproduced biogas can be recycled again to cultivate the neededmicroalgal biomass for processing [107110ndash112]

A predicted model of microalgae biomass for digestion toproduce electrical and thermal energy discussed the economicprofitability related with technical aspects of the productionsystem The results showed that the microalgae productivityharvesting concentration and usage of high rate anaerobic diges-ters are the key factors for the economic energy production [113]

A life cycle perspective study using a stochastic model indi-cated that when compared with the conventional crops likeswitch grass canola and corn the environmental impact ofmicroalgal biomass production is higher with respect to energydemand greenhouse gas emissions and water use regardless ofcultivation location Only in overall land use and eutrophicationpotential microalgae present favorable results [114] This mayseem to be a disadvantage to produce biomethane from microalgalbiomass but the studies also supported that the integratedprocesses using proper photobioreactors combining microalgaecultivation and waste water treatment systems for biomethaneproduction will help to reduce the environmental impacts result-ing in a competitive and effective production [11416115]

25 Integrated processes

Relations between parameters and the target products (bio-mass lipid hydrogen ethanol) are important in the selection ofthe microalgae for efficient biofuel production As can be followedfrom the tables summarizing the microalgal biofuel productions

Sugars

- Sugarcane juice

- Molasses

- Sugar beet

Starch

- Corn

- Oats

- Wheat

- Sago Palm

- Cassava

- Banana wastes

- Rye

- Barley

- Triticale

- Sorghum

- Algal biomass

Lignocellulosic materials

- Crop residues

- Cellulose wastes

- Hardwood

- Harbaceous biomass

- Softwood

- Municipal solid wastes

Fermentation

- Saccharomyces cerevisiae

- Schizosaccharomyces pombe

- Zymomonas mobilis

- Saccharomyces bayanus

- Pichia stipitis

- Candida shehatae

- Pachysolen tannophilus

- Mucor indicus

- Chalara parvispora

- T thermosaccharolyticum

- T Ethanolicus

- B Stearothermophilus

- C thermohydrosulfuricum

- C thermocellum

- Milling

- Grinding

- ShredingBreaking hemicellulose

chains

- Physical

- Chemical

- Physicochemical

- Biological

Hydrolization -Detoxification

-Neutralization

Sugars

- Hexoses

- Pentoses

Separation and

Concentration

- Distillation

- Rectification

- Dehydration

ETHANOL

Fig 4 Ethanol production from biomass productionSource Adapted from Refs [9398201]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 253

studies focus on the separation of production processes into twomain steps growth mediated and product mediated When con-sidering direct biofuel production the main approach is product

mediated for higher lipid hydrogen or ethanol production Whenconsidering biofuel production integrated with other microorgan-isms (Table 5) the main approach is growth mediated for higher

Table 5Integrated biofuel processes working with microalgae

Microalgae System Product Ref

Chlamydomonas reinhardtii (UTEX 90) Enzymatic treatment of algal biomass and conversion to ethanol by Saccharomyces cerevisiae Ethanol [179]Chlamydomonas reinhardtii (UTEX 90) Hydrothermal acid treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [180]Chlorella vulgaris (IAM C-534) Enzymatic treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [181]Synechococcus leopoliensis (IAMM 6) Fermentation of acid treated saccharified algal biomass by yeast Saccharomyces sake (IFO 2347) Ethanol [97]Chlamydomonas reinhardtii Chlorella vulgaris (macroalgae Undaria pinnatifida) Enzymatic treatment of pre-acid hydrolyzed algal biomass fermentation by 4 different strains of Escherichia coli Ethanol [182]Schizocytrium sp Fermentation of hydrothermal treated algal biomass by E coli KO11 Ethanol [183]Microcystis aeruginosa and Anabaena variabilis Hydrolysis and fermentation of Super Critical fluid pretreated algal biomass by Saccharomyces cerevisiae Ethanol [204]Scenedesmus obliquus Fermentation of algal biomass hydrolysate by Kluyveromyces marxianus IGC 2671 Saccharomyces carlsbergensis

ATCC6269 and Saccharomyces bayanusEthanol [205]

Anabaena sp PCC7120 Fermentation of hydrogen produced residual algal biomass by Enterobacter aerogenes Hydrogen [184]Arthrospira (Spirulina) platensis Nannochloropsis sp and Dunaliella tertilecta Anaerobic fermentation of thermal pretreated algal biomass by immobilized Clostridium acetobutylicum Hydrogen acetone

ethanol butanol[206]

Chlorella vulgaris ESP6 Dark fermentation of acid or alkalineenzyme pretreated algal biomass hydrolysate by Clostridium butyricumCGS5

Hydrogen [207]

Chlorella sp Simultaneous hydrolysis and fermentation of algal biomass by sewage sludge consortia Hydrogen [208]Thalassiosira weissflogii Dark fermentation of algal biomass with the thermophilic bacterium Thermotoga neapolitana Hydrogen [209]Chlamydomonas reinhardtii (IAM C-238) Chlorella pyrenoidosa (IAM C-212) andDunaliella tertiolecta (ATCC 30909)

Fermentation of algal biomass by Lactobacillus amylovorous (ATCC 33620) and Rhodobacter sphaeroides RV Hydrogen [185]

Chlamydomonas reinhardtii (IAM C-238) and Dunaliella tertiolecta (ATCC 30909) Fermentation of algal biomass by Lactobacillus amylovorous and Rhodobium marinum (A-501) mixed culture Hydrogen [186]Chlamydomonas (MGA 161) Fermentation of algal biomass by Rhodovulum sulfidophilum (W-1S) Hydrogen [85]Chlamydomonas reinhardtii (C238) Mixed cultivation of Chlamydomonas reinhardtii (C238) with Rhodospirillum rubrum (NCIB 8255) Hydrogen [187]Scnedesmus sp Fermentation of algal biomass by anaerobic digested sludge Hydrogen [188]Arthrospira maxima Anaerobic digestion of algal biomass by sewage sludge consortia Methane [210]Phaeodactylum tricornutum Anaerobic digestion of algal biomass by potato factory origin anaerobic granular sludge Methane [211]Scenedesmus sp Anaerobic digestion of high pressure thermal pretreated raw and residue (from lipid extraction) algal biomass

and by anaerobic digestor sludgeMethane [212]

Scenedesmus sp Anaerobic digestion of ultrasound and thermal pretreated raw algal biomass by sugar factory origin anaerobicgranular sludge

Methane [213]

Scenedesmus sp Anaerobic digestion of mild thermal pretreated raw algal biomass by sugar factory origin anaerobic granularsludge

Methane [214]

Spirulina platensis Anabaena variabilis and Chlorella sp Processing of algal biomass by an integrated system of methanogenic culture and Rhodobacter capsulatus Methane and hydrogen [189]Spirulina platensis (UTEX 1926) Rhodotorula glutinis (2541) Mixed cultivation of microalgae and yeast using waste water Lipid (biodiesel) [190]Spirulina platensis Using excess CO2 from the ethanol fermentation by Saccharomyces cerevisiae Lipid (biodiesel) [119]Botryococcus braunii (two strains BB763 and BB764) Chlorella vulgaris Chlorellapyrenoidosa

Biodiesel production catalyzed by immobilized Penicillium expansum lipase and Candida antarctica lipase B(Novozym 435)

Lipid (biodiesel) [191]

Chlorella vulgaris (21111B) Anaerobic digestion of algal biomass by sewage sludge origin methanogenic culture Methane [112]Chlorella sp and Scenedesmus Anaerobic digestion of algal biomass by sewage sludge culture Methane [106]Chlorella sp Anaerobic digestion of algal biomass by sludge culture Methane [192]Arthrospira platensis Chlamydomonas reinhardtii Chlorella kessleri Dunaliellasalina Euglena gracilis and Scenedesmus obliquus

Anaerobic digestion of algal biomass by sewage sludge culture Methane [107]

Spirulina maxima Anaerobic digestion of algal biomass by sewage sludge culture Methane [193]Chlorella sp and Scenedesmus Anaerobic codigestion of algal biomass with waste paper by methanogenic culture Methane [194]Tetraselmis Anaerobic digestion of algal biomass by methanogenic culture Methane [195]Chlorococcum sp Anaerobic treatment of distillery waste with algal biomass by acidogenicmethanogenic culture Methane [196]Phaeodactylum tricornutum (CCAP10551) Anaerobic digestion of algal biomass by granular seed sludge from digester treating potato processing waste

water dominated by Methanosaeta sp and Methanosarcina spMethane [197]

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biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

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technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

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[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

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[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

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[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

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[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

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[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

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[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

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[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

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[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

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[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

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[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

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[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

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[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

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[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 13: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

Sugars

- Sugarcane juice

- Molasses

- Sugar beet

Starch

- Corn

- Oats

- Wheat

- Sago Palm

- Cassava

- Banana wastes

- Rye

- Barley

- Triticale

- Sorghum

- Algal biomass

Lignocellulosic materials

- Crop residues

- Cellulose wastes

- Hardwood

- Harbaceous biomass

- Softwood

- Municipal solid wastes

Fermentation

- Saccharomyces cerevisiae

- Schizosaccharomyces pombe

- Zymomonas mobilis

- Saccharomyces bayanus

- Pichia stipitis

- Candida shehatae

- Pachysolen tannophilus

- Mucor indicus

- Chalara parvispora

- T thermosaccharolyticum

- T Ethanolicus

- B Stearothermophilus

- C thermohydrosulfuricum

- C thermocellum

- Milling

- Grinding

- ShredingBreaking hemicellulose

chains

- Physical

- Chemical

- Physicochemical

- Biological

Hydrolization -Detoxification

-Neutralization

Sugars

- Hexoses

- Pentoses

Separation and

Concentration

- Distillation

- Rectification

- Dehydration

ETHANOL

Fig 4 Ethanol production from biomass productionSource Adapted from Refs [9398201]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 253

studies focus on the separation of production processes into twomain steps growth mediated and product mediated When con-sidering direct biofuel production the main approach is product

mediated for higher lipid hydrogen or ethanol production Whenconsidering biofuel production integrated with other microorgan-isms (Table 5) the main approach is growth mediated for higher

Table 5Integrated biofuel processes working with microalgae

Microalgae System Product Ref

Chlamydomonas reinhardtii (UTEX 90) Enzymatic treatment of algal biomass and conversion to ethanol by Saccharomyces cerevisiae Ethanol [179]Chlamydomonas reinhardtii (UTEX 90) Hydrothermal acid treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [180]Chlorella vulgaris (IAM C-534) Enzymatic treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [181]Synechococcus leopoliensis (IAMM 6) Fermentation of acid treated saccharified algal biomass by yeast Saccharomyces sake (IFO 2347) Ethanol [97]Chlamydomonas reinhardtii Chlorella vulgaris (macroalgae Undaria pinnatifida) Enzymatic treatment of pre-acid hydrolyzed algal biomass fermentation by 4 different strains of Escherichia coli Ethanol [182]Schizocytrium sp Fermentation of hydrothermal treated algal biomass by E coli KO11 Ethanol [183]Microcystis aeruginosa and Anabaena variabilis Hydrolysis and fermentation of Super Critical fluid pretreated algal biomass by Saccharomyces cerevisiae Ethanol [204]Scenedesmus obliquus Fermentation of algal biomass hydrolysate by Kluyveromyces marxianus IGC 2671 Saccharomyces carlsbergensis

ATCC6269 and Saccharomyces bayanusEthanol [205]

Anabaena sp PCC7120 Fermentation of hydrogen produced residual algal biomass by Enterobacter aerogenes Hydrogen [184]Arthrospira (Spirulina) platensis Nannochloropsis sp and Dunaliella tertilecta Anaerobic fermentation of thermal pretreated algal biomass by immobilized Clostridium acetobutylicum Hydrogen acetone

ethanol butanol[206]

Chlorella vulgaris ESP6 Dark fermentation of acid or alkalineenzyme pretreated algal biomass hydrolysate by Clostridium butyricumCGS5

Hydrogen [207]

Chlorella sp Simultaneous hydrolysis and fermentation of algal biomass by sewage sludge consortia Hydrogen [208]Thalassiosira weissflogii Dark fermentation of algal biomass with the thermophilic bacterium Thermotoga neapolitana Hydrogen [209]Chlamydomonas reinhardtii (IAM C-238) Chlorella pyrenoidosa (IAM C-212) andDunaliella tertiolecta (ATCC 30909)

Fermentation of algal biomass by Lactobacillus amylovorous (ATCC 33620) and Rhodobacter sphaeroides RV Hydrogen [185]

Chlamydomonas reinhardtii (IAM C-238) and Dunaliella tertiolecta (ATCC 30909) Fermentation of algal biomass by Lactobacillus amylovorous and Rhodobium marinum (A-501) mixed culture Hydrogen [186]Chlamydomonas (MGA 161) Fermentation of algal biomass by Rhodovulum sulfidophilum (W-1S) Hydrogen [85]Chlamydomonas reinhardtii (C238) Mixed cultivation of Chlamydomonas reinhardtii (C238) with Rhodospirillum rubrum (NCIB 8255) Hydrogen [187]Scnedesmus sp Fermentation of algal biomass by anaerobic digested sludge Hydrogen [188]Arthrospira maxima Anaerobic digestion of algal biomass by sewage sludge consortia Methane [210]Phaeodactylum tricornutum Anaerobic digestion of algal biomass by potato factory origin anaerobic granular sludge Methane [211]Scenedesmus sp Anaerobic digestion of high pressure thermal pretreated raw and residue (from lipid extraction) algal biomass

and by anaerobic digestor sludgeMethane [212]

Scenedesmus sp Anaerobic digestion of ultrasound and thermal pretreated raw algal biomass by sugar factory origin anaerobicgranular sludge

Methane [213]

Scenedesmus sp Anaerobic digestion of mild thermal pretreated raw algal biomass by sugar factory origin anaerobic granularsludge

Methane [214]

Spirulina platensis Anabaena variabilis and Chlorella sp Processing of algal biomass by an integrated system of methanogenic culture and Rhodobacter capsulatus Methane and hydrogen [189]Spirulina platensis (UTEX 1926) Rhodotorula glutinis (2541) Mixed cultivation of microalgae and yeast using waste water Lipid (biodiesel) [190]Spirulina platensis Using excess CO2 from the ethanol fermentation by Saccharomyces cerevisiae Lipid (biodiesel) [119]Botryococcus braunii (two strains BB763 and BB764) Chlorella vulgaris Chlorellapyrenoidosa

Biodiesel production catalyzed by immobilized Penicillium expansum lipase and Candida antarctica lipase B(Novozym 435)

Lipid (biodiesel) [191]

Chlorella vulgaris (21111B) Anaerobic digestion of algal biomass by sewage sludge origin methanogenic culture Methane [112]Chlorella sp and Scenedesmus Anaerobic digestion of algal biomass by sewage sludge culture Methane [106]Chlorella sp Anaerobic digestion of algal biomass by sludge culture Methane [192]Arthrospira platensis Chlamydomonas reinhardtii Chlorella kessleri Dunaliellasalina Euglena gracilis and Scenedesmus obliquus

Anaerobic digestion of algal biomass by sewage sludge culture Methane [107]

Spirulina maxima Anaerobic digestion of algal biomass by sewage sludge culture Methane [193]Chlorella sp and Scenedesmus Anaerobic codigestion of algal biomass with waste paper by methanogenic culture Methane [194]Tetraselmis Anaerobic digestion of algal biomass by methanogenic culture Methane [195]Chlorococcum sp Anaerobic treatment of distillery waste with algal biomass by acidogenicmethanogenic culture Methane [196]Phaeodactylum tricornutum (CCAP10551) Anaerobic digestion of algal biomass by granular seed sludge from digester treating potato processing waste

water dominated by Methanosaeta sp and Methanosarcina spMethane [197]

SSOncel

Renew

ableand

SustainableEnergy

Review

s26

(2013)241

ndash264254

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 255

biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264256

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

SSOncel

Renew

ableand

SustainableEnergy

Review

s26

(2013)241

ndash264258

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 259

technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

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[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264262

[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 14: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

Table 5Integrated biofuel processes working with microalgae

Microalgae System Product Ref

Chlamydomonas reinhardtii (UTEX 90) Enzymatic treatment of algal biomass and conversion to ethanol by Saccharomyces cerevisiae Ethanol [179]Chlamydomonas reinhardtii (UTEX 90) Hydrothermal acid treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [180]Chlorella vulgaris (IAM C-534) Enzymatic treatment of algal biomass and conversion fermentation by Saccharomyces cerevisiae Ethanol [181]Synechococcus leopoliensis (IAMM 6) Fermentation of acid treated saccharified algal biomass by yeast Saccharomyces sake (IFO 2347) Ethanol [97]Chlamydomonas reinhardtii Chlorella vulgaris (macroalgae Undaria pinnatifida) Enzymatic treatment of pre-acid hydrolyzed algal biomass fermentation by 4 different strains of Escherichia coli Ethanol [182]Schizocytrium sp Fermentation of hydrothermal treated algal biomass by E coli KO11 Ethanol [183]Microcystis aeruginosa and Anabaena variabilis Hydrolysis and fermentation of Super Critical fluid pretreated algal biomass by Saccharomyces cerevisiae Ethanol [204]Scenedesmus obliquus Fermentation of algal biomass hydrolysate by Kluyveromyces marxianus IGC 2671 Saccharomyces carlsbergensis

ATCC6269 and Saccharomyces bayanusEthanol [205]

Anabaena sp PCC7120 Fermentation of hydrogen produced residual algal biomass by Enterobacter aerogenes Hydrogen [184]Arthrospira (Spirulina) platensis Nannochloropsis sp and Dunaliella tertilecta Anaerobic fermentation of thermal pretreated algal biomass by immobilized Clostridium acetobutylicum Hydrogen acetone

ethanol butanol[206]

Chlorella vulgaris ESP6 Dark fermentation of acid or alkalineenzyme pretreated algal biomass hydrolysate by Clostridium butyricumCGS5

Hydrogen [207]

Chlorella sp Simultaneous hydrolysis and fermentation of algal biomass by sewage sludge consortia Hydrogen [208]Thalassiosira weissflogii Dark fermentation of algal biomass with the thermophilic bacterium Thermotoga neapolitana Hydrogen [209]Chlamydomonas reinhardtii (IAM C-238) Chlorella pyrenoidosa (IAM C-212) andDunaliella tertiolecta (ATCC 30909)

Fermentation of algal biomass by Lactobacillus amylovorous (ATCC 33620) and Rhodobacter sphaeroides RV Hydrogen [185]

Chlamydomonas reinhardtii (IAM C-238) and Dunaliella tertiolecta (ATCC 30909) Fermentation of algal biomass by Lactobacillus amylovorous and Rhodobium marinum (A-501) mixed culture Hydrogen [186]Chlamydomonas (MGA 161) Fermentation of algal biomass by Rhodovulum sulfidophilum (W-1S) Hydrogen [85]Chlamydomonas reinhardtii (C238) Mixed cultivation of Chlamydomonas reinhardtii (C238) with Rhodospirillum rubrum (NCIB 8255) Hydrogen [187]Scnedesmus sp Fermentation of algal biomass by anaerobic digested sludge Hydrogen [188]Arthrospira maxima Anaerobic digestion of algal biomass by sewage sludge consortia Methane [210]Phaeodactylum tricornutum Anaerobic digestion of algal biomass by potato factory origin anaerobic granular sludge Methane [211]Scenedesmus sp Anaerobic digestion of high pressure thermal pretreated raw and residue (from lipid extraction) algal biomass

and by anaerobic digestor sludgeMethane [212]

Scenedesmus sp Anaerobic digestion of ultrasound and thermal pretreated raw algal biomass by sugar factory origin anaerobicgranular sludge

Methane [213]

Scenedesmus sp Anaerobic digestion of mild thermal pretreated raw algal biomass by sugar factory origin anaerobic granularsludge

Methane [214]

Spirulina platensis Anabaena variabilis and Chlorella sp Processing of algal biomass by an integrated system of methanogenic culture and Rhodobacter capsulatus Methane and hydrogen [189]Spirulina platensis (UTEX 1926) Rhodotorula glutinis (2541) Mixed cultivation of microalgae and yeast using waste water Lipid (biodiesel) [190]Spirulina platensis Using excess CO2 from the ethanol fermentation by Saccharomyces cerevisiae Lipid (biodiesel) [119]Botryococcus braunii (two strains BB763 and BB764) Chlorella vulgaris Chlorellapyrenoidosa

Biodiesel production catalyzed by immobilized Penicillium expansum lipase and Candida antarctica lipase B(Novozym 435)

Lipid (biodiesel) [191]

Chlorella vulgaris (21111B) Anaerobic digestion of algal biomass by sewage sludge origin methanogenic culture Methane [112]Chlorella sp and Scenedesmus Anaerobic digestion of algal biomass by sewage sludge culture Methane [106]Chlorella sp Anaerobic digestion of algal biomass by sludge culture Methane [192]Arthrospira platensis Chlamydomonas reinhardtii Chlorella kessleri Dunaliellasalina Euglena gracilis and Scenedesmus obliquus

Anaerobic digestion of algal biomass by sewage sludge culture Methane [107]

Spirulina maxima Anaerobic digestion of algal biomass by sewage sludge culture Methane [193]Chlorella sp and Scenedesmus Anaerobic codigestion of algal biomass with waste paper by methanogenic culture Methane [194]Tetraselmis Anaerobic digestion of algal biomass by methanogenic culture Methane [195]Chlorococcum sp Anaerobic treatment of distillery waste with algal biomass by acidogenicmethanogenic culture Methane [196]Phaeodactylum tricornutum (CCAP10551) Anaerobic digestion of algal biomass by granular seed sludge from digester treating potato processing waste

water dominated by Methanosaeta sp and Methanosarcina spMethane [197]

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biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

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technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

[1] EIA (US Energy Information Administration) International Energy Outlook2010 Washington DC 20585 US 2010 langwwweiagovoiafieoindexhtmlrang

[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264262

[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 15: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 255

biomass production The idea of integration is to unite each systemin a way that both processes will complete each other in order tohave a higher productivity and lower cost using all the sourcesincluding waste and excess streams

A good example is the usage of bioethanol from renewablesources rather than using the petroleum based methanol for agreener approach and to complete the real biofuel idea Comparedto ethanolysis toxicity the risk of vapor explosion due to metha-nols low boiling point lower oxidative stability higher iodinevalue and higher exhaust emissions are other motivations behindethanol usage Fatty acid ethyl esters have similar properties tomethyl esters and the ethanolysis reaction can also work withvarious feedstocks utilizing catalytic and non-catalytic reactionslike conventional methanolysis [11689117] The cost will be themain limit but biorefinery concept can overcome the constraints

Other than the direct bioethanol usage for biodiesel produc-tion the integration of large scale microalgal cultivation withethanol biorefineries to use the excess CO2 to grow microalgaewhich can then be used as feedstock for biofuel production is alsonoteworthy An economic evaluation study for Iowa USA pointedthat selecting a good candidate strain like Chlorella vulgaris can befeasible and profitable when integrated with bioethanol refineries[118] A similar approach for the utilization of excess CO2 fromethanol fermentation was investigated to be feasible for theproduction of Spirulina platensis for lipid production [119] andkeeping in mind that the residual algal biomass can be recycledagain to the fermentation process this integration will be promis-ing Also the integration of the microalgae production systemswith sugar mill facilities will help to share the excess CO2 watermolasses and energy from the boilers that will be advantageousfor the process feasibility [120]

Considering the environmental impact co-culturing microalgaewith methane oxidizing bacterial communities utilizes the excessCO2 allowing a methane oxidation with minimum emission Onthe other hand the produced oxygen through photosynthesislowers the need of external O2 to maintain methane oxidationby 55 This approach will have potential for large scale anaerobicwaste water plants which will reduce two important greenhousegases CH4 and CO2 in a single process [121]

Valorization of the excess glycerol from the biodiesel and CO2

for glycerol carbonate production is a good alternative for theeconomic benefit of biodiesel production [122]

An economic study indicates that the microalgae residues frombiodiesel production that will be used in biomethane productionfor electricity generation will make the production of biodieselfrom algae more competitive by reducing the overall productioncosts especially energy needs for downstream processes [123]

Using microalgae for waste water bioremediation targetingbiofuel production has potential for daily life application [124] Aconceptual design of Green Wisdom Inc USA using microalgaefor integrated bioremediation and biofuel production showed thepotential of microalgae for rural communities economic accelera-tion and sustainability A successful integration can decreasebiofuel costs and valuable microalgal by-products may help theproduction costs to be competitive On the other hand using CO2

and waste water the microalgae can improve the environmentalload with regard to pollution and achieve more sustainable living[125]

26 Light to fuel

Starting with strain isolation microalgae proceed throughdifferent process steps until the final product is obtained (Fig 5)Even if these steps are well adapted in commercial scale processesbased on biomass production for some species [23517] micro-algae production still needs development for the key processes

such as pretreatment production modes photobioreactor designdownstream techniques and energy demand to be more effectivesustainable productive and environmentally friendly [4181974114115]

Amongst the immense species of microalgae there is anopportunity for finding a candidate having a potential to be usedfor biofuel Also contrary with the diversity few strains of focus isanother factor that increases the possibility Realization of thebiofuel production depends on the specie which should beselected according to the target product Focusing on the targetwhich is microalgal biofuel production the process from light tofuel can be divided into two levels laboratory and industrial

Laboratory is the main unit where necessary investigationsfrom culture conditions to design can be done with multipleexperiments that simulate the effects of different parameters likelight mixing temperature and aeration on the production to getrealistic potential of the microalgae with regard to biofuel produc-tion Targeting the industrial scale all the data starting with thetest tubes should be transferred step by step to flasks and later tophotobioreactors where online control of the process can behandled and possible modifications can be done to increase theproduction Being of diverse types photobioreactor is a tool forscale-up that should be investigated in detail considering all thepros and cons [2126ndash129] Photobioreactors will help to mimicinteractive scenarios faced with the larger systems in a controlledenvironment ensuring an objective comparison among all typesOn the other hand in the downstream processes another keyfeature of the microalgal fuel process can be investigated inlaboratory scale to evaluate their application efficiency andharmony with the whole process Again various applications andmethods for separation concentration extraction and purificationcan be compared to have a higher productivity in industrialprocess [4182172] After the detailed investigation consideringall the steps from the test tube to the photobioreactor stage withthe entire downstream process one can have a clear idea about thepotential of the microalgae for biofuel production

The bridge from laboratory to industry is the scale-up thatplays a vital role in commercialization There are different strate-gies for the scale-up depending on various factors The idea is todetermine a constant value for a parameter of a unit volume that isassumed to represent the whole system which is in other wordsindependent from the scale These factors include operationalparameters like mixing time gas transfer rates dissolved gasconcentration mixer blade tip velocity linear velocity lightintensity per illuminated area light intensity per volume Reynoldsnumber and Power number and dimensional parameters likeillumination area culture volume ratio height to diameter ratioand blade diameter to tank diameter ratio [2372737691129]Especially in the case of photobioreactors to develop a successfulscale-up strategy it is necessary to consider both operational anddimensional parameters Again a strong background investigationon laboratory basis will warrant a successful scale-up

After the development of the scale-up strategy the laboratoryknowledge is ready to be transferred to large scale cultivationsBecause large scale productions have extra complexity for man-agement related with the increased dimensions of the systemsthey may need different methods of approach to solve theproblems compared to small laboratory productions Entire pro-cess from photobioreactors to downstream systems must be scaledup maintaining the harmony for high productivities

Other than the physical part of the system design increase inscale will also necessitate the economical investigation of theprocess [45113] Even if the economy seemed to be shaded inlaboratory scales it is the actual motivation of the whole processthat targets a valuable product to have an economic benefit Asuccessfully scaled-up process should also be feasible and

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264256

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

SSOncel

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ableand

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Review

s26

(2013)241

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SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 259

technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

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[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

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[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

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[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

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[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

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[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

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[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

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[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

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[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 16: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

Microalgae

bull Isolation from naturebull Dilution and production in small multi celled platesbull Cell selection and sorting through agar culturesbull Transfer of single cells to small volume test tubes for suspension culturesbull Transfer to the higher volumes (Erlenmayer flasks)

Small scale (flasks)

bull Mimicing their natural habitat for cultivation (temperature nutrientslight) bull Analytical investigation of their potential regrads to the product (pigments lipid bio active compounds etc)

bull Experiments for the determination of the culture conditions for the target product (nutrients pH temperature illumination strategy (continuous LD cycles) culture modes (autotrophic mixotrophic heterotrophic) mixing regime (turbulent laminar))

bull Experimental design for the optimization of culture conditions for highest productivitybull Transfering the data based on erlenmayer trials to photobioreactor experiments

Photobioreactors

bull Utilization of different designs (tubular (helical fence conical curved) panel (torous rectangular baffled) column (bubble airlift divided external) stirred tank (multi blade baffled) focusing on their pros and cons for the highest productivity and applicability

bull Choosing the proper photobioreactors under optimized conditions comparing the productivities and application to larger scales

bull Investigation of the down stream systems (separation concentration drying disruption extraction purification) having the best efficiency considering the production as a whole

bull Experiments for culture regimes (batch continuous fed batch) control strategies (direct cascade)

bull Modifications on the design (blade type spager type aeration (bubble or bubble free) illumination (internal external) light source (daylight cool white colored) illumination system (Lamps LED optic fiber fluorescent tubes reflectors) if necessary

bull Determination of the key features for scale-up (mixing regime light intensity temperature pH aeration)

Scale -up

bull Focusing on the scale-up strategy considering unit volume (dissolved O2 dissolved CO2 kLa mixing time blade tip velocity illumination area culture volume relation light intensity relation between area and volume optical path)

bull Investigation of the efficient down stream processes for the highest product keeping in mind the large scale productions

bull Productions from lab scale to pilot scale step by step regards to constants (DO kLatime etc) considering control strategies

bull Transfering the process to outdoors and investigation of the productivity interacting with climate (sun light daily cycle temperature variation clouds etc)

bull Annual examination and observation of the productions to have the clear idea about the productivity

bull Modifications of the design according to the needs (sprays for temp control sun shields to prevent light inhibition efficient aeration systems etc)

Industrial production

bull Investigation simulation and adaptation of the pilot scale data using engineering tools (CAD models LCA etc) to the industrial scale considering all the physical modifications blending with the econometric criterias (market prices operation transportation maintanence costs etc) to have a feasible and profit process

bull Construction of the industrial scale facility again increasing the units step by step to secure the income and expenditure balance

bull Life long RampD activities to protect the dynamism of the facility considering product development biorefineries waste treatment

Fig 5 From light to bioproduct considering the basic process steps

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264256

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

SSOncel

Renew

ableand

SustainableEnergy

Review

s26

(2013)241

ndash264258

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 259

technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

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[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

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[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

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[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

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[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

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[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

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[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

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[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

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[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

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[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

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[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

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[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

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[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 17: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 257

profitable as well as have high productivity through a welldesigned system based on the knowledge from laboratory to theoutdoors

27 Future prospects

Focusing on the light to fuel concept the main concerns aboutthe future are based on the bottlenecks of microalgae productionswhich can be surpassed with the advantages that are pointed outby various researchers [79114126ndash134]

Requirement of large areas for outdoor scales with considerableamount of water This problem can be solved by the cultivationon lands like desert arid and semi-arid lands using salinebrackish water or coastal seawater

Limited species of interest Because they are research friendlywith the possibility of laboratory scale production there is achance for rapid investigation of new species Using photobior-eactors culture conditions can be controlled for the needs ofthe studied microalga in order to understand its specificationsand potential This way especially the limited outdoor produc-tions based on environment and contamination tolerant spe-cies can be spread to other species

Limited outdoor applications in large scales with regard tosystems and dependency on weather The background knowl-edge about their biomass targeted large scale open pondcultivations and development of diversified new designs ofphoto-bioreactors considering CO2 feed illumination and mix-ing efficiencies and preventing evaporation losses will accel-erate the applications Also because the microalgae can betransferred using conventional pipelines mass productions canbe done in areas with proper climate and transferred to otherplaces for further applications which may lower the produc-tion costs especially in the case of biofuels

Nutrient requirement like phosphorus that is becoming scarceEspecially the utilization of waste waters and by-products fromother conventional processes like flue gases organic carboncontaining wastes may help the production to be feasible andsustainable

Need progress in downstream processes to lower the produc-tion costs Working on the new separation and extractionsystems with higher efficiencies gives promising results forfuture applications

Unclear cost per volume compared to fossil fuels with regard toa market price Considering their faster growth compared toterrestrial plants their higher biomass productivity on arealbasis and a better adaptation to elevated CO2 and nutrientlevels microalgae has a high potential to be produced in vastamounts with appropriate selection of the species and produc-tion systems Modification of their biochemical composition bysimple changes in their cultivation conditions (nutrients lightintensity temperature mixing etc) for higher productivities ofthe targeted products is another advantage On the other handtheir ability to synthesize and accumulate various high valueproducts (eg biopolymers proteins polysaccharides pig-ments) will help to reduce the production costs and supportthe feasibility Keeping in mind their useful adaptation with thebiorefineries high potential for carbon credits and efficientblending with liquid fuels operational costs besides the pro-duction costs can be decreased to competitive prices Theprogresses in material science and technology will also helpproducers utilize the proper equipment with lower cost

Low production levels with regard to biofuels to compete withthe fossil fuels can be solved with the developed productionand downstream systems to some point Also the progress ingenetic engineering to understand the cellular production

mechanisms and the modifications in molecular basis is pro-mising for future scenarios On the other hand utilization ofphotobioreactors increases the productivities of various speciesby controlling the culture conditions and eliminatingcontaminations

However the key is to get realistic projections without exag-gerating the potential Because of this microalgae based biofuelsshould be objectively handled to have a clear vision of the futureMain challenge is the realization of the microalgal biofuel usageconsidering present and future targets (Table 6)

Today several turnkey applications are presenting the dynamicprogress of the microalgal energy Algenol Company aimed toeliminate the separation and extraction costs and had promisingresults from patented process for ethanol secreting microalgaeusing outdoor photobioreactors without harvesting and killing themicroalgae just someway milking it Also Origin Oil anothercompany has patented a novel single step extraction process inwhich the biomass water and oil is separated continuously with-out chemicals The company is now transferring the knowhow forlarge scale productions Keeping in mind the integrated applica-tions NASA with its OMEGA project has planned to producemicroalgae offshore in large sea farms utilizing elastic bag typephotobioreactors This way the land costs will be limited themicroalgae cultured with waste water and flue gases will help toprevent pollution and using osmosis technology cleaned waterwill be separated from microalgae that will help for the feasibleproduction of biofuels fertilizers and food Joule Energy geneti-cally engineered a microalga like microorganism to secrete lipidhydrocarbons in a single step process eliminating all downstreamprocesses and producing ready-for-energy biofuel

Microalgal biofuels may not become a direct competitor tofossil fuels in near future but can be an alternative at some areasAccording to EIA liquid fuels will continue to dominate the worldmarketed energy use In future scenarios when considering oilprices the change will mainly affect the consumption of liquidfuels which are the key features in transportation [1] This can be agood opportunity for microalgal biofuels where they can find alane to grow Microalgae based biodiesel and bioethanol have thepotential to be used directly or as a blend for internal combustionengines while biohydrogen can be used in green diesel productionor in the fuel celled vehicles which will orient the microalgalbiofuels to our daily life On the other hand their potential to beused as a support with the conventional fuels is an importantroute for the economic benefit Also to have feasible investmentand production costs the contribution for improved biofuel pro-duction by specialized strains with higher yields which areapplicable for outdoor cultivations and integrated processes withother microorganisms serves a realistic strategy for sustainableproduction To reach the goals for the future economy of todayshould be considered

3 Economy

The main concern of the economy which is also its drivingforce can be summarized as the balance of the massive contesta-tion between the earths limited resources and the humans end-less appetite for progress sometimes far more than the needsFrom the bioeconomy point of view with regard to microalgalfuels this can be depicted as the interrelation between the cost ofthe production and the revenue from sale keeping in mind thecompetitiveness with other fossil fuels

To produce all microalgae based fuels one should first producethe microalgae The road to feasibility passes from the well-established and analyzed production costs related with

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

SSOncel

Renew

ableand

SustainableEnergy

Review

s26

(2013)241

ndash264258

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 259

technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

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[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

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[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

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[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

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[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

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[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

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[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

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[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 18: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

Table 6The constraints future targets and comments-opinions for microalgal biofuel realization

Focus Today Target Commentsopinions

Microalgae Few strains in focus variable productivitiesmore interest from other sectors likepharmaceutical aquaculture etc ratherthan energy

Selection of new strains and routes for maximizedproductivities with regard to biofuel

Genetically modified strains can have a chance for higher productions but the key is to control theirpossible effects on nature and determination of their applications with legislations New species will alsobe discovered and used in researches for progress Also rather than the monoculture processes mixed orco-cultures of microalgae with other microorganisms will increase the chance of application

Photobioreactors Limited large scale productions highinvestment costs depending on thetechnical and constructional needs

Improved designs considering outdoor productionsinteractive with environment lower production cost

Outdoor open ponds will be used in the future but with the improving materials and constructiontechniques they can be transformed to closed systems with feasible modifications for increasedproductivity with diverse species On the other hand two basic designs tubular and panel will also findcommercial application as a support unit that may be used for more sophisticated by products todecrease the production cost of the biofuels produced by pond systems

Microalgalbiofuels

Limited usage but increasing interest withthe progress in fuel cell technology engineshydrogen storage microalgae oilethanolproduction and extraction severalproduction steps

Higher productivities with single step processesleading to daily life usage in areas like transportation

Considering its potential biodiesel will be the dominator over the other microalgal biofuels But keepingin mind the bioethanol and biomethane production through integrated processes they can be a supportfor the economic feasibility of the biodiesel process by using its residues and recycle streamsBiohydrogen can be classified separately with its potential to be used in fuel cells

Biorefineries Beginning of the spread usage withbiorefinery concept

Stronger biorefinery attitude with the corporationof residential and industrial facilities supported withproduction of biomass and biofuels as by-products

Like petroleum refineries gaining all the possible products will be an advantage for microalgae that hasdiverse by-products in addition to biofuel important for different sectors The key is the integration withother conventional bioprocesses like fermentation digestion and waste treatment

Economy Variable feasibility depending on theproduction process and technology

Feasible production considering improveddownstream processes new photobioreactor designsand carbon credits

Other than the economic profit from the biofuel producing by-products through biorefinery concept willhelp to decrease the operational costs Possible integration with other commercial processes excessemissions energy and waste can be used in the productions serving as an economic advantage Alsotransporting microalgae through conventional pipelines can be an advantage for the production insuitable climates and refinement of the raw biomass in specified facilities elsewhere will decrease thecost of downstream processes This way the producers can send their product to centralize refinementfacilities to eliminate extra infrastructure similar to the refineries in the petroleum industry Microalgaebased biofuels will also act as a backup to control the prices of especially petroleum when the reservesstart to deplete resulting in big price sway with regard to elevated oil concession and drilling costs

Energy Limited share in renewables and limiteddaily life usage

Higher share widespread usage Energy from coal hydro and nuclear will continue to dominate the massive demand But depending onthe petroleum prices microalgal biofuels can increase their share especially in the area of transportationBiodiesel and bioethanol will get the main attention as blends with petroleum whereas biohydrogenwith fuel celled cars

SSOncel

Renew

ableand

SustainableEnergy

Review

s26

(2013)241

ndash264258

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 259

technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

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[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264262

[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 19: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 259

technology which also serve a fertile ground for future researchand development for new industries Based on the main costcomponents that add up to the total cost a process shouldconsider the cost of land (yard improvement roads etc) productionsystems (buildings service facilities storage silos open pond orphotobioreactor inoculation nutrient delivery control sterilizationcooling heating pumping aeration and mixing units) harvestingsystems (centrifuges filters settling tanks conveyors dryers etc)downstream systems (homogenization disruption extraction andpurification units) and operational expenses (management main-tenance labor electricity purchase insurance employee trainingtransportation consumables and taxes) [215ndash222] Any progress todecrease the cost in these components where research and devel-opment expenses are also important is a challenge and motivationfor researchers and entrepreneurs

The key is to have an objective estimation of the unit cost ofproduction in order to foresee the market value The economicbackground of production mainly built on the conventionalmarkets of health food feed and valuable chemicals especiallyrelated to cosmeceuticals or pharmaceuticals The cost of produc-tion with regard to these markets is in the range of 1ndash7$ kgminus1 ofraw algal biomass [5128223224] depending on the productionprocess But these values may rise up to 1000$ kgminus1 (2) especiallyin the case of utilizing sophisticated systems including photobior-eactors and downstream equipment for example in the produc-tions related with pharmaceutical industry However one shouldalso consider that the revenue of such a high cost will also payhigh For example some biochemicals have high price like ldquoastax-anthinrdquo from Haematococcus has a price up to 10000$ kgminus1 orldquoβ-carotenerdquo from Dunaliella has a price up to 3000$ kgminus1 depend-ing on the purity and quality in the world market [225]

Similar to the conventional markets the main point in the costof fuel production as mentioned is also related with the processFor microalgae the challenge is to compete both with fuel cropsand fossil fuels with regard to the unit cost

Considering the case of biodiesel or green diesel according tothe average prices for April 2013 [226] algal oil which can be usedshould not exceed the prices of its competitors vegetable oils(palm soybean rapeseed sunflower) with an average density of091 kgLminus1 [227] around 07ndash13$ Lminus1 petroleum (West TexasDubai Brent) around 059ndash064$ Lminus1 and petroleum diesel around076ndash085$ Lminus1 Blending these selling prices with the cost ofmicroalgae biomass production Chisti (5128) foresaw a cost of034$ kgminus1 as a limit for feasible production yielding a cost of 280$ Lminus1 for algal oil This assumption depending on the 55 oilcontent per biomass weight is still realistic for today to competepetroleum diesel because of the relative productivity of thespecies Other than the importance of the selected species theaverage cost of microalgal oil under compatible conditions (withan oil content of about 30 of biomass free CO2 low cost ofnutrients and 114 L kgminus1 oil extraction capability) is estimated as295$ Lminus1 in open ponds while it needs to be enhanced to 38$ Lminus1

in the photobioreactors [228] to reach the feasible limitsOn the other hand similar approaches for market feasibility can

be accepted for ethanol which has a price of 067$ Lminus1 or forhydrogen production based on water electrolysis that has anaverage value depending on the electricity price 3ndash118$ kgminus1 also[226228]

On the economic aspect the utilization of open ponds orphotobioreactors and the downstream steps should be wellevaluated A case study with tubular type photobioreactor toproduce high value intracellular oils from marine microalgaPhaeodactylum tricornutum showed that the key points for afeasible production are based on the production and recovery ofthe biomass extraction of oils from the wet biomass and purifica-tion of the crude extract The average cost of producing biomass

was 3216$ kgminus1 the crude esterified oil was 39652$ kgminus1 whilethis cost stepped up to 4602$ kgminus1 after purification This hugedifference marked an overall cost profile of 40 that resulted frombiomass production and 60 from recovery [215] To overcomethese high costs different scenarios of biofuel production withregard to integrated processes aiming wastewater treatment andbiofuels production showed that the best cost will be around 302$ barrelminus1 which is still very high compared to petroleum [216]Another cost pricing study estimates a value microalgal oil(1 barrelfrac1442 US gal) to be 356$ barrelminus1 for open pond and 760$ barrelminus1 for photobioreactor productions On upgrading to greendiesel via hydrotreatment these costs will elevate to 413$ barrelminus1

and 863$ barrelminus1 [217] which are still far beyond even the averageselling prices of petroleum diesel which are about 122ndash135$ barrelminus1

Despite all these values microalgal biofuels can still be the vitalsolution for the replacement or support to fossil fuels Thecompanies are continuously investing millions of dollars forresearch and realization After delivering 80000 L of algal dieselto US navy in 2010 multi-million dollar company Solazyme hasanother contract of about extra 550000 L Also they haveannounced in March 2013 the results of consumer survey as thefeedback of a partnership with a leading fuel retailer that 92 ofthe consumers are interested in using algae based biodiesel againin their vehicles instead of fossil fuels considering environmentalissues Also another company Sapphire has scaled up its process to100 acres by 2013 targeting a capacity of 1 million barrels of crudealgal oil per year in a full 300 acres facility On the other handSynthetic Genomics has a deal with Exxon for about $600 millionfor the realization of motor fuels from algae back in 2009 Thisimmense amount was planned as the key for developmentAccording to Bloomberg Business in 2013 Exxon is still interestedin the business even if the venture was prolonged to 25 yearsrather than their first prediction of 10 years till commercialization

These update news are prosperous for the future of microalgaebased fuels even if there is still some time to feasibility Never-theless knowing inevitable reality of the vanishing fossil fuelreserves in the next century and the conflict of fuel cropscompeting with food crops microalgae that have the ability toutilize the colossal energy of the sun will have a clear future

4 Ethical issues

Similar to all other fuels from raw to product the ethical issuesare also important for the microalgal biofuels The need for abetter world for humanity with regard to environment andeconomy without omitting fair and secure distribution of energyis the motivation for the bioenergy and bioeconomy The key totake a strong step to realization depends on the ethical valuesconsidering human rights justice solidarity sustainability andstewardship [229ndash231] To fulfill the ethical needs microalgaebased biofuels have some advantages over other conventionalfuels First of all they will not interfere with the food and waterthat are essential for humanity with their ability to live in variousenvironments They are environmentally more sustainable withregard to their ability to utilize sun even flue gases and wastewaters This will also help to reduce the net greenhouse gasemissions to limit global warming besides water treatment Theycan be adapted and integrated with conventional fuel refineriesinfra-structure and trade principles in order to have a smoothtransform to a real bioeconomy Last but not the least with theirvarious by-products and production systems microalgae can act asleverage for labor inter-generational equity and resilience in thesociety [229ndash233]

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

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[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

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[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

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[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 20: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264260

On the other hand again similar to the other fuels the mainconcern is the controlled progress in order to minimize theenvironmental impacts especially with regard to production landConsumption of space may cause problems with the local habitatThis risk will be higher if alien species or genetically modifiedspecies are utilized Also a vicious cycle will be formed if thepetroleum based fertilizers and gases will be utilized withoutoptimization causing a continuation in petroleum dependencyAnother risk of using fertilizers is the runoff of the culture processstreams resulting in uncontrolled eutrophication in water systemsThese points should be well focused for prevention because theywill contradict with ethical issues that will damage the reliabilityof the microalgal fuels On the global basis the maturation of theindustry should be well coordinated and controlled not to face anychaos Also to prevent monopolization research and developmentshould be public focused and respect human rights fulfilling theconcept of fair trade [229ndash231]

We have to think for today and tomorrow considering the nextgenerations and the shared welfare and equity will be relatedwith the diversification of the energy sources and reducing thedependency on fossil fuels in which microalgae will be a promis-ing candidate

5 Conclusions

Combining the background knowledge of their biology andculture production microalgae diversity producing various valu-able bioproducts is an advantage Also the commercial interestwith the rising awareness for environmental and energy issues arestrong catalysers for the progress

Today we come to a point where nothing seems to be solved ina quick and easy way Environmental problems versus energystruggle force us to choose a pathway for sustainable future Oneway is to continue on the vast consumption of natural resourcesthereby increasing the problems Another way is to change our oldhabits and focus on the sustainable and environmentally friendlylifestyle starting with the consumption of energy

Biofuels started with the first generation continuing with thesecond and the third and leading today to the fourth generationfocusing on the modified organisms with low carbon impact willcontinue to evolve with the changes of the world needs andpriorities

Based on the economic consideration microalgae productionsystems and facilities are required to be well planned for a feasibleproduction strategy Even though it seems to face cost crisismarketing and commercialization hardships for todays worldthe relief in the ethical issues related to microalgae biofuelproduction starts a new era for clean sustainable and environ-mental friendly production for future

Even if microalgal biofuels seem to be a rookie compared to thefossil fuels their baby steps may have a chance to get faster only ifwe can analyze their potential realistically

In the attempt to have a better world microalgae contrary totheir name may have a macroimpact on progress

References

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[2] Pulz O Gross W Valuable products from biotechnology of microalgaeApplied Microbiology and Biotechnology 200465635ndash48

[3] Eriksen NT The technology of microalgal culturing Biotechnology Letters2008301525ndash36

[4] Spolaore P Cassan CJ Duran E Isambert A Commercial applications ofmicroalgae Journal of Bioscience and Bioengineering 200610187ndash96

[5] Chisti Y Biodiesel from microalgae Biotechnology Advances 200725294ndash306

[6] Wijffels RH Barbosa MJ An outlook on microalgal biofuels Science2010329796ndash9

[7] Aikins GP Nadim A El-Halwagi MM Mahalec V Design and analysis ofbiodiesel production from algae grown through carbon sequestration CleanTechnologies and Environmental Policy 201012239ndash54

[8] Knothe G Biodiesel and renewable diesel a comparison Progress in Energyand Combustion Science 201036364ndash73

[9] Hu Q Sommerfeld M Jarvis E Ghirardi M Posewitz M Seibert M et alMicroalgal triacylglycerols as feedstocks for biofuel production perspectivesand advances The Plant Journal 200854621ndash39

[10] Sharma YC Singh B Upaghyay SN Advancements in development andcharacterization of biodiesel a review Fuel 2008872355ndash73

[11] Hoekman SK Broch A Robbins C Ceniceros E Natarajan M Review ofbiodiesel composition properties and specifications Renewable amp Sustain-able Energy Reviews 201216143ndash69

[12] Chen YH Huang BY Chiang TH Tang TC Fuel properties of microalgae(Chlorella protothecoides) oil biodiesel and its blends with petroleum dieselFuel 201294270ndash3

[13] Griffiths MJ Harrison STL Lipid productivity as a key characteristic forchoosing algal species for biodiesel production Journal of Applied Phycology200921493ndash507

[14] Yoo C Jun SY Lee JY Ahn CY Oh HM Selection of microalgae for lipidproduction under high levels of carbon dioxide Bioresource Technology201010171ndash4

[15] Tran HL Kwon JS Kim ZH Oh Y Lee CG Statistical optimization of culturemedia for growth and lipid production of Botryococcus braunii LB572Biotechnology Biopro Engineering 201015277ndash84

[16] Pienkos PT Darzins A The promise and challenges of microalgal-derivedbiofuels Biofuels Bioproducts and Biorefining 20093431ndash40

[17] Harun R Singh M Forde GM Danquah MK Bioprocess engineering ofmicroalgae to produce a variety of consumer products Renewable ampSustainable Energy Reviews 2010141037ndash47

[18] Mercer P Armenta RE Developments in oil extraction from microalgaeEuropean Journal of Lipid Science and Technology 2011113539ndash47

[19] Halim R Danquah MK Webley PA Extraction of oil from microalgae forbiodiesel production a review Biotechnology Advances 201230709ndash32

[20] Yusuf NNAN Kamrudin SK Yaakub Z Overview on the current trends inbiodiesel production Energy Conversion Management 2011522741ndash51

[21] Teixeira RE Energy-efficient extraction of fuel and chemical feedstocks fromalgae Green Chemistry 201214419ndash27

[22] Orta VSB Lee JGM Harvey A Alkaline in situ transesterification of Chlorellavulgaris Fuel 201294544ndash50

[23] Lee JY Yoo C Jun SY Ahn CY Oh HM Comparison of several methods foreffective lipid extraction from microalgae Bioresource Technology 2010101S75ndashS77

[24] Halim R Harun R Danquah MK Webley PA Microalgal cell disruption forbiofuel development Applied Energy 201291116ndash21

[25] Medina AR Moreno PAG Cerdaacuten LE Grima EM Biocatalysis towards evergreener biodiesel production Biotechnology Advances 200927398ndash408

[26] Akoh CC Chang SW Lee GC Shaw JF Enzymatic approach to biodieselproduction Journal of Agricultural and Food Chemistry 2007558995ndash9005

[27] Murugesan A Umarani C Chinnusamy TR Krishnan M Subramanian RNeduzchezhain N Production and analysis of bio-diesel from non-edible oilsmdasha review Renewable amp Sustainable Energy Reviews 200913825ndash34

[28] Demirbas A Biodiesel production from vegetable oils via catalytic and non-catalytic supercritical methanol transesterification methods Progress inEnergy and Combustion Science 200531466ndash87

[29] Yin JZ Xiao M Song JB Biodiesel from soybean oil in supercritical methanolwith co solvent Energy Conversion and Management 200849908ndash12

[30] Shahid EM Jamal Y Production of biodiesel a technical review Renewable ampSustainable Energy Reviews 2011154732ndash45

[31] Diego TD Manjon A Lozano P Iborra JL A recyclable enzymatic biodieselproduction process in ionic liquids Bioresource Technology 20111026336ndash9

[32] Bajaj A Lohan P Jha PN Mehrotra R Biodiesel production through lipasecatalyzed transesterification an overview Journal of Molecular Catalysis BEnzymatic 2010629ndash14

[33] Gog A Roman M Tos M Paizs C Irimie FD Biodiesel production usingenzymatic transesterificationmdashcurrent state and perspectives RenewableEnergy 20123910ndash6

[34] Zhang B Weng Y Xu H Mao Z Enzyme immobilization for biodieselproduction Applied Microbiology and Biotechnology 20129361ndash70

[35] Hama S Tamalampudi S Yoshida A Tamadania N Kuratanic N Noda H et alEnzymatic packed-bed reactor integrated with glycerol-separating systemfor solvent-free production of biodiesel fuel Biochemical EngineeringJournal 20115566ndash71

[36] Devi PBLA Guo Z Xu X Characterization of ionic liquid-based biocatalytictwo-phase reaction system for production of biodiesel AIChE Journal2011571628ndash37

[37] Du W Xu Y Liu D Zeng J Comparative study on lipase-catalyzed transfor-mation of soybean oil for biodiesel production with different acyl acceptorsJournal of Molecular Catalysis B Enzymatic 200430125ndash9

[38] Jeon DJ Yeom SH Comparison of methods for preventing methanol inhibi-tion in enzymatic production of biodiesel Korean Journal of ChemicalEngineering 2011281420ndash6

[39] Talukder MMR Wu JC Fen NM Melissa YLS Two-step lipase catalysis forproduction of biodiesel Biochemical Engineering Journal 201049207ndash12

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264262

[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 21: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 261

[40] Li L Du W Liu D Wang L Li Z Lipase-catalyzed transesterification ofrapeseed oils for biodiesel production with a novel organic solvent as thereaction medium Journal of Molecular Catalysis B Enzymatic20064358ndash62

[41] Demirbas A Biodiesel from sunflower oil in supercritical methanol withcalcium oxide Energy Conversion and Management 200748937ndash41

[42] Zhong J Xiao M Song JB Biodiesel from soybean oil in supercriticalmethanol with co-solvent Energy Conversion and Management200849908ndash12

[43] Eisenmenger MJ Corcuera JIR High pressure enhancement of enzymes areview Enzyme and Microbial Technology 200945331ndash47

[44] Wimmer Z Zarevucka M A review on the effects of supercritical carbondioxide on enzyme activity International Journal of Molecular Science201011233ndash53

[45] Jegannathan RK Seng EC Ravindra P Economic assessment of biodieselproduction comparison of alkali and biocatalyst processes Renewable ampSustainable Energy Reviews 201115745ndash51

[46] McNeff CV McNeff LC Yan B Nowlan DT Rasmussen M Gyberg AE et al Acontinuous catalytic system for biodiesel production Applied Catalysis A200834339ndash48

[47] Um BH Kim YS Review a chance for Korea to advance algal-biodieseltechnology Journal of Industrial and Engineering Chemistry 2009151ndash7

[48] Krohn BJ McNeff CV Yan B Nowlan D Production of algae-based biodieselusing the continuous catalytic Mcgyan process Bioresource Technology201110294ndash100

[49] Radakovits R Jinkerson RE Fuerstenberg SI Tae H Settlage RE Boore JL et alDraft genome sequence and genetic transformation of the oleaginous algaNannochloropis gaditana Nature Communications 201210 httpdxdoiorg101038ncomms1688

[50] Day JG Slocombe SP Stanley MS Overcoming biological constraints toenable the exploitation of microalgae for biofuels Bioresource Technology2012109245ndash51

[51] Steen EJ Kang Y Bokinsky G Hu Z Schirmer A McClure SBC et al Microbialproduction of fatty-acid-derived fuels and chemicals from plant biomassNature 2010463559ndash62

[52] Larkum AWD Ross IL Kruse O Hankamer B Selection breeding andengineering of microalgae for bioenergy and biofuel production Trends inBiotechnology 201230198ndash205

[53] Das D Veziroglu TN Advances in biological hydrogen production processesInternational Journal of Hydrogen Energy 2008336046ndash57

[54] Kim MS Baek JS Yun YS Sim SJ Park S Kim SC Hydrogen production fromChlamydomonas reinhardtii biomass using a two-step conversion processanaerobic conversion and photosynthetic fermentation International Jour-nal of Hydrogen Energy 200631812ndash6

[55] Nath K Das D Hydrogen from biomass Current Science 200385265ndash71[56] Gaffron H Reduction of carbon dioxide with molecular hydrogen in green

algea Nature 1939143204ndash5[57] Hallenbeck PC Benemann JR Biological hydrogen production fundamentals

and limiting processes International Journal of Hydrogen Energy2002271185ndash93

[58] Momirlan M Veziroglu T Recent directions of world hydrogen productionRenewable amp Sustainable Energy Reviews 19933219ndash31

[59] Levin DB Pitt L Love M Biohydrogen production prospects and limitationsto practical application International Journal of Hydrogen Energy200429173ndash85

[60] Das D Veziroglu TN Hydrogen production by biological processes a surveyof literature International Journal of Hydrogen Energy 20012613ndash28

[61] Kovacs KL Maroti G Rakhely G A novel approach for biohydrogen produc-tion International Journal of Hydrogen Energy 2006311460ndash8

[62] Benemann JR Hydrogen production by microalgae Journal of AppliedPhycology 200012291ndash300

[63] Masukawa H Mochimaru M Sakurai H Hydrogenases and photobiologicalhydrogen production utilizing nitrogenase system in cyanobacteria Interna-tional Journal of Hydrogen Energy 2002271471ndash4

[64] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[65] Kojima E Lin B Effect of partial shading on photoproduction of hydrogen byChlorella Journal of Bioscience and Bioengineering 200497317ndash21

[66] Guan Y Zhang W Deng M Jin YuX Significant enhancement of photo-biological H2 evolution by carbonylcyanide m-chlorophenylhydrazone in themarine green alga Platymonas subcordiformis Biotechnology Letters2004261031ndash5

[67] Guan Y Deng M Yu X Zhang W Two-stage photo-biological production ofhydrogen by marine green alga Platymonas subcordiformis BiochemicalEngineering Journal 20041969ndash73

[68] Aoyama K Uemura I Miyake J Asada Y Fermentative metabolism to producehydrogen gas and organic compounds in a cyanobacterium Spirulinaplatensis Journal of Fermentation and Bioengineering 19978317ndash20

[69] Melis A Zhang L Forestier M Ghirardi ML Seibert M Sustained photo-biological hydrogen gas production upon reversible inactivation of oxygenevolution in the green alga Chlamydomonas reinhardtii Plant Physiology2000122127ndash35

[70] Melis A Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (uni-cellular green algae) Planta 20072261075ndash86

[71] Kosourov S Makarova V Fedorov AS Tsygankov A Seibert M Ghirardi MLThe effect of sulfur re-addition on H2 photoproduction by sulfur-deprivedgreen algae Photosynthesis Research 200585295ndash305

[72] Eroglu E Melis A Photobiological hydrogen production recent advances andstate of the art Bioresource Technology 20111028403ndash13

[73] Melis A Photosynthesis-to-fuels from sunlight to hydrogen isoprene andbotryococcene production Energy amp Environmental Science 201255531ndash9

[74] Lindblad P The potential of using cyanobacteria as producers of molecularhydrogen In Miyake J Igarashi Y Rogner M editors Biohydrogen renew-able energy system by biological solar energy conversion London ElsevierPress 2004 p 75ndash82

[75] Madamwar D Garg N Shah V Cyanobacterial hydrogen production WorldJournal of Microbiology amp Biotechnology 200016757ndash67

[76] Dasgupta CN Gilbert JJ Lindblad P Heidorn T Borgvang SA Skjanes K et alRecent trends on the development of photobiological processes and photo-bioreactors for the improvement of hydrogen production InternationalJournal of Hydrogen Energy 20103510218ndash38

[77] Stripp ST Happe T How algae produce hydrogen news from the photosyn-thetic hydrogenase Dalton Transactions 2009459960ndash9

[78] Polle JWE Kanakagiri S Jin ES Masuda T Melis A Truncated chlorophyllantenna size of the photosystems a practical method to improve microalgalproductivity and hydrogen production in mass culture International Journalof Hydrogen Energy 2002271257ndash64

[79] Rupprecht J Hankamer B Mussgnug JH Ananyev G Dismukes C Kruse OPerspectives and advances of biological H2 production in microorganismsApplied Microbiology and Biotechnology 200672442ndash9

[80] Vijayaraghavan K Karthik R Nalini Kamala SP Hydrogen production byChlamydomonas reinhardtii under light driven sulfur deprived conditionInternational Journal of Hydrogen Energy 2009347964ndash70

[81] Gaffron H Rubin J Fermentative and photochemical production of hydrogenin algae Journal of General Physiology 194226219ndash40

[82] Homann PH Hydrogen metabolism of green algae discovery and earlyresearch a tribute to Hans Gaffron and his coworkers PhotosynthesisResearch 20037693ndash103

[83] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiI Analysis of fermentative products from starch in dark and light PlantPhysiology 198475212ndash8

[84] Gfeller RP Gibbs M Fermentative metabolism of Chlamydomonas reinhardtiiII Role of plastoquinone Plant Physiology 198577509ndash11

[85] Miura Y Akano T Fukatsu K Miyasaka H Mizoguchi T Yagi K et al Stablysustained hydrogen production by biophotolysis in natural daynight cycleEnergy Conversion and Management 199738533ndash7

[86] Wykoff DD Davies JP Melis A Grossman AR The regulation of photosyn-thetic electron transport during nutrient deprivation in Chlamydomonasreinhardtii Plant Physiology 1998117129ndash39

[87] Laurinavichene T Tolstygina I Tsygankov A The effect of light intensity onhydrogen production by sulfur-deprived Chlamydomonas reinhardtii Journalof Biotechnology 2004114143ndash51

[88] Kima JP Kang CD Park TY Kim MS Sim SJ Enhanced hydrogen productionby controlling light intensity in sulfur deprived Chlamydomonas reinhardtiiculture International Journal of Hydrogen Energy 2006311585ndash90

[89] Zhang Y Fan X Yang Z Wang H Yang D Guo R Characterization of H2

photoproduction by a new marine green alga Platymonas helgolandica varTsingtaoensis Applied Energy 20129238ndash43

[90] Philipps G Happe T Hemschemeier A Nitrogen deprivation results inphotosynthetic hydrogen production in Chlamydomonas reinhardtii Planta2012235729ndash45

[91] Scoma A Giannelli L Faraloni C Torzillo G Outdoor H2 production in a 50-Ltubular photobioreactor by means of a sulfur-deprived culture of the micro-alga Chlamydomonas reinhardtii Journal of Biotechnology 2012157620ndash7

[92] Mathews J Wang G Metabolic pathway engineering for enhanced biohydro-gen production International Journal of Hydrogen Energy 2009347404ndash16

[93] John RP Anisha GS Nampoothiri KM Pandey A Micro and macroalgalbiomass a renewable source for bioethanol Bioresource Technology2011102186ndash93

[94] Hirayama S Ueda R Ogushi Y Hirano A Samejima Y Hon-Nami K et alEthanol production from carbon dioxide by fermentative microalgae Studiesin Surface Science and Catalysis 1998114657ndash60

[95] Bush RA Hall KM Process for the production of ethanol from algae USPatent 7135308 2006

[96] Ueda R Hirayama S Sugata K Nakayama H Process for the production ofethanol from microalgae US Patent 5578472 1996

[97] Mustaqim D Ohtaguchi KA Synthesis of bioreactions for the production ofethanol from CO2 Energy 199722353ndash6

[98] Mussatto SI Dragone G Guimaratildees PMR Silva JPA Carneiro LM Roberto ICet al Technological trends global market and challenges of bio-ethanolproduction Biotechnology Advances 201028817ndash30

[99] Kurano Ueno Y Miyachi S Ethanol production by dark fermentation in themarine green alga Chlorococcum littorale Journal of Fermtation and Bioen-gineering 19988638ndash43

[100] Klein U Betz A Fermentative metabolism of hydrogen evolving Chlamydo-monas moewusii Plant Physiology 197861953ndash6

[101] Syrett PJ Wong HA The fermentation of glucose by Chlorella vulgarisBiochemical Journal 196389308ndash15

[102] Stal LJ Moezelaar R Fermentation in cyanobacteria FEMS MicrobiologyReviews 199721179ndash211

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[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 22: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264262

[103] Troshina O Serebryakova L Sheremetieva M Lindblad P Production of H2 bythe unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermen-tation International Journal of Hydrogen Energy 2002271283ndash9

[104] Deng MD Coleman JR Ethanol synthesis by genetic engineering in cyano-bacteria Applied and Environmental Microbiology 199965523ndash8

[105] Lou D Hu Z Choi DG Thomas VM Real MJ Chance RR Life cycle energy andgreenhouse gas emissions for an ethanol production process based on blue-green algae Environmental Science and Technology 2010448670ndash7

[106] Golueke CG Oswald WJ Gotaas HB Anaerobic digestion of algae AppliedMicrobiology 1957547ndash55

[107] Mussgnug JH Klassen V Schluumlter A Kruse O Microalgae as substrates forfermentative biogas production in a combined biorefinery concept Journal ofBiotechnology 201015051ndash6

[108] Schenk PM Hall SRT Stephens E Marx UC Mussgnug JH Posten C et alSecond generation biofuels high-efficiency microalgae for biodiesel produc-tion Bioenergy Research 2008120ndash43

[109] Fernandez AV Vargas G Alarcon N Velasco A Evaluation of marine algae as asource of biogas in a two-stage anaerobic reactor system Biomass ampBioenergy 200832338ndash44

[110] Douskova I Kastanek F Maleterova Y Kastanek P Doucha J Zachleder VUtilization of distillery stillage for energy generation and concurrent produc-tion of valuable microalgal biomass in the sequence biogas-cogeneration-microalgae-products Energy Conversion and Management 201051606ndash11

[111] Ras M Lardon L Bruno S Bernet N Steyer JP Experimental study on acoupled process of production and anaerobic digestion of Chlorella vulgarisBioresource Technology 2011102200ndash6

[112] Chynoweth DP Fannin FK Srivastava JV Biological gasification of marinemicroalgae In Bird KT Benson PH editors Seaweed cultivation for renew-able resources Amsterdam Elsevier Press 1987 p 287ndash303

[113] Zamalloa C Vulsteke E Albrecht J Verstraete W The techno-economicpotential of renewable energy through the anaerobic digestion of microalgaeBioresource Technology 20111021149ndash58

[114] Clarens AF Resurreccion EP White MA Colosi AM Environmental life cyclecomparison of algae to other bioenergy feedstocks Environmental Scienceand Technology 2010441813ndash9

[115] Jorquera O Kiperstok A Sales EA Embiruccedilu M Ghirardi ML Comparativeenergy life-cycle analyses of microalgal biomass production in open pondsand photobioreactors Bioresource Technology 20101011406ndash13

[116] Stamenkovic OS Velikovic AV Veljkovic VB The production of biodiesel fromvegetable oils by ethanolysis current state and perspectives Fuel2011903141ndash55

[117] Brunschwig C Moussavou W Blin J Use of bioethanol for biodiesel produc-tion Progress in Energy and Combustion Science 201238283ndash301

[118] Rosenberg JN Mathias A Korth K Betenbaugh MJ Oyler GA Microalgalbiomass production and carbon dioxide sequestration from an integratedethanol biorefinery in Iowa a technical appraisal and economic feasibilityevaluation Biomass amp Bioenergy 2011353865ndash76

[119] Ferreira LS Rodrigues MS Converti A Sato S Carvalho JCM Arthrospira(Spirulina) platensis cultivation in tubular photobioreactor use of no-costCO2 from ethanol fermentation Applied Energy 201292379ndash85

[120] Lohrey C Kochergin V Biodiesel production from microalgae co-locationwith sugar mills Bioresource Technology 201210876ndash82

[121] Ha D Bundervoet B Verstrate W Boon N A sustainable carbon neutralmethane oxidation by a partnership of methane oxidizing communities andmicroalgae Water Research 2011452845ndash54

[122] Gomez JRO Aberasturi GJ Lopez CR Belsue M A brief review on industrialalternatives for the manufacturing of glycerol carbonate a green chemicalOrganic Process Research amp Development 201216389ndash99

[123] Harun R Davidson M Doyle M Gopiraj R Danquah M Forde M Technoe-conomic analysis of an integrated microalgae photobioreactor biodiesel andbiogas production facility Biomass amp Bioenergy 201135741ndash7

[124] Rawat I Kumar RR Mutanda T Bux F Dual role of microalgae phycoreme-diation of domestic wastewater Applied Energy 2011883411ndash24

[125] Sivakumar G Xu J Thompson RW Yang Y Smith PR Weathers PJ Integratedgreen algal technology for bioremediation and biofuel Bioresource Technol-ogy 20121071ndash9

[126] Stephenson AL Kazamia E Dennis JS Howe CJ Scott SA Smith AG Life-cycleassessment of potential algal biodiesel production in the United Kingdom acomparison of raceways and air-lift tubular bioreactors Energy Fuels2007244062ndash77

[127] Lehr F Posten C Closed photo-bioreactors as tools for biofuel productionCurrent Opinion in Biotechnology 200920280ndash5

[128] Chisti Y Biodiesel from microalgae beat bioethanol Trends in Biotechnology200826126ndash31

[129] Hankamer B Lehr F Rupprecht J Mussgnug JH Posten C Kruse O Photo-synthetic biomass and H2 production by green algae from bioengineering tobioreactor scale-up Physiologia Plantarum 200713110ndash21

[130] Roumlsch C Skarka J Wegerer J Materials flow modeling of nutrient recycling inbiodiesel production from microalgae Bioresource Technology 2012107191ndash9

[131] Liu X Clarens AF Colosi LM Algae biodiesel has potential despite incon-clusive results to date Bioresource Technology 2012104803ndash6

[132] Vasudevan V Stratton RW Pearlson MN Jersey GR Beyene AG Weissman JCet al Environmental performance of algal biofuel technology optionsEnvironmental Science and Technology 2012462451ndash9

[133] Lam MK Lee KT Microalgae biofuels a critical review of issues problemsand the way forward Biotechnology Advances 201230673ndash90

[134] Petkov G Ivanova A Iliev I Vaseva I A critical look at the microalgaebiodiesel European Journal of Lipid Science and Technology 2012114103ndash11

[135] Medina AR Grima EM Gimenez A Gonzales MJI Downstream processing ofalgal polyunsaturated fatty acids Biotechnology Advances 199816517ndash80

[136] Vilchez C Garbayo I Lobato MV Vega JM Microalgae-mediated chemicalsproduction and wastes removal Enzyme and Microbial Technology199720562ndash72

[137] Huerlimann R Nys R Heimann K Growth lipid content productivity andfatty acid composition of tropical microalgae for scale-up productionBiotechnology and Bioengineering 2010107245ndash57

[138] Li Y Horsman M Wu N Lan CQ Calero ND Biofuels from microalgaeBiotechnology Progress 200824815ndash20

[139] Singh J Gu S Commercialization potential of microalgae for biofuelsproduction Renewable amp Sustainable Energy Reviews 2010142596ndash610

[140] Comprehensive Oilgae Report Preview Energy from Algae Products MarketProcesses amp Strategies Available at langhttpwwwoilgaecomrefreportoilgae_reportshtmlrang 2010

[141] Edward M The algal industry survey a white paper by Dr Mark Edward ampCentre for management technology Available at langwwwascension-publishingcomBIZalgal-industry-surveypdfrang 2009

[142] Kloeck G Microalgae internet directory Available at langhttpwwwrenewableenergyworldcomreablogpost201008a-microalgae-industry20internet-directoryrang 2010

[143] Ge Y Liu J Tian G Growth characteristics of Botryococcus braunii 765 underhigh CO2 concentration in photobioreactor Bioresource Technology2011102130ndash4

[144] Ruangsomboon S Effect of light nutrient cultivation time and salinity onlipid production of newly isolated strain of the green microalga Botryococcusbraunii KMITL 2 Bioresource Technology 2012109261ndash5

[145] Kong Q Li L Martinez B Chen P Ruan R Culture of microalgae Chlamydo-monas reinhardtii in wastewater for biomass feedstock production AppliedBiochemistry and Biotechnology 20101609ndash18

[146] Converti A Casazza AA Ortiz EY Perego P Borghi MD Effect of temperatureand nitrogen concentration on the growth and lipid content of Nannochlor-opsis oculata and Chlorella vulgaris for biodiesel production ChemicalEngineering and Processing 2009481146ndash51

[147] Hongjin Q Guangce W Effect of carbon source on growth and lipidaccumulation in Chlorella sorokiniana GXNN01 Chinese Journal of Oceanol-ogy and Limnology 200927762ndash8

[148] Oh SH Kwon MC Choi WY Seo YC Kim GB Kang DH et al Long-termoutdoor cultivation by perfusing spent medium for biodiesel productionfrom Chlorella minutissima Journal of Bioscience and Bioengineering2010110194ndash200

[149] Arroyo TH Wei W Hu B Oil accumulation via heterotrophicmixotrophicChlorella protothecoides Applied Biochemistry and Biotechnology 20101621978ndash95

[150] Sforza E Cipriani R Morosinotto T Bertucco A Giacometti GM Excess CO2

supply inhibits mixotrophic growth of Chlorella protothecoides and Nanno-chloropsis salina Bioresource Technology 2012104523ndash9

[151] Wang H Xiong H Hui Z Zeng X Mixotrophic cultivation of Chlorellapyrenoidosa with diluted primary piggery wastewater to produce lipidsBioresource Technology 2012104215ndash20

[152] Hongyang S Yalei Z Chunmin Z Xuefei Z Jinpeng L Cultivation of Chlorellapyrenoidosa in soybean processing wastewater Bioresource Technology20111029884ndash90

[153] Hu B Min M Zhou W Li Y Mohr M Cheng Y et al Influence of exogenousCO2 on biomass and lipid accumulation of microalgae Auxenochlorellaprotothecoides cultivated in concentrated municipal wastewater AppliedMicrobiology and Biotechnology 20121661661ndash73

[154] Lv JM Cheng LH Xu XH Zhang L Chen HL Enhanced lipid production ofChlorella vulgaris by adjustment of cultivation conditions Bioresource Tech-nology 20101016797ndash804

[155] Doucha J Livansky K Production of high-density Chlorella culture grown infermenters Journal of Applied Phycology 20122435ndash43

[156] Pribyl P Cepak V Zachleder V Production of lipids in 10 strains of Chlorellaand Parachlorella and enhanced lipid productivity in Chlorella vulgarisApplied Microbiology and Biotechnology 201294549ndash61

[157] Sobczuk TM Chisti Y Potential fuel oils from the microalga Choricystisminor Journal of Chemical Technology and Biotechnology 201085100ndash8

[158] Park SJ Choi YE Kim EJ Park WK Kim CW Yang JW Serial optimization ofbiomass production using microalga Nannochloris oculata and correspondinglipid biosynthesis Bioprocess and Biosystems Engineering 2012353ndash9

[159] Damiani MC Popovich CA Constenla D Leonardi PI Lipid analysis inHaematococcus pluvialis to assess its potential use as a biodiesel feedstockBioresource Technology 20101013801ndash7

[160] Li Y Horsman M Wang B Wu N Lan CQ Effects of nitrogen sources on cellgrowth and lipid accumulation of green alga Neochloris oleoabundansApplied Microbiology and Biotechnology 200881629ndash36

[161] Gouveia L Marques AE Silva TL Reis A Neochloris oleabundans UTEX 1185a suitable renewable lipid source for biofuel production Journal of IndustrialMicrobiology amp Biotechnology 200936821ndash6

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 23: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264 263

[162] Pruvost J Van Vooren G Cogne V Legrand J Investigation of biomass andlipids production with Neochloris oleoabundans in photobioreactor Biore-source Technology 20091005988ndash95

[163] Go S Lee SJ Jeong GW Kim SK Factors affecting the growth and the oilaccumulation of marine microalgae Tetraselmis suecica Bioprocess andBiosystems Engineering 201235145ndash50

[164] Markov SA Thomas AD Bazin MJ Hall DO Photoproduction of hydrogen bycyanobacteria under partial vacuum in batch culture or in a photobioreactorInternational Journal of Hydrogen Energy 199722521ndash4

[165] Tsygankov AS Serebryakova LT Svesnikov DA Rao KK Gogotov IN Hall DOHydrogen photoproduction by three different nitrogenases in whole cells ofAnabaena variabilis and the dependence on pH International Journal ofHydrogen Energy 199722859ndash67

[166] Lindblad P Christensson K Lindberg P Fedorov A Pinto F Tsygankov APhotoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogenuptake deficient mutant from laboratory experiments to outdoor cultureInternational Journal of Hydrogen Energy 2002271271ndash81

[167] Yoon JH Shin JH Kim MS Sim SJ Park TH Evaluation of conversion efficiencyof light to hydrogen energy by Anabaena variabilis International Journal ofHydrogen Energy 200631721ndash7

[168] Tsygankov A Kosourov S Seibert M Ghirardi ML Hydrogen photoproductionunder continuous illumination by sulfur-deprived synchronous Chlamydo-monas reinhardtii cultures International Journal of Hydrogen Energy2002271239ndash44

[169] Fedorov AS Kosourov S Ghirardi MI Seibert M Continuous hydrogenphotoproduction by Chlamydomonas reinhardtii using a novel two-stagesulfate-limited chemostat system Applied Biochemistry and Biotechnology2005121403ndash12

[170] Laurinavichene TV Fedorov AS Ghirardi ML Seibert M Tsygankov ADemonstration of sustained hydrogen photoproduction by immobilizedsulfur-deprived Chlamydomonas reinhardtii cells International Journal ofHydrogen Energy 200631659ndash67

[171] Kosourov S Patrusheva E Ghirardi ML Seibert M Tsygankov A A comparison ofhydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii underdifferent growth conditions Journal of Biotechnology 2007128776ndash87

[172] Tolstygina IV Antal TK Kosourov SN Krendeleva TE Rubin AB Tsygankov AAHydrogen production by photoautotrophic sulfur-deprived Chlamydomonasreinhardtii pre-grown and incubated under high light Biotechnology andBioengineering 20091021055ndash61

[173] Oncel S Vardar-Sukan F Photo-bioproduction of hydrogen by Chlamydomo-nas reinhardtii using a semi-continuous process regime International Journalof Hydrogen Energy 2009347592ndash602

[174] Kosourov SN Seibert M Hydrogen photoproduction by nutrient-deprivedChlamydomonas reinhardtii cells immobilized within thin alginate films underaerobic and anaerobic conditions Biotechnology and Bioengineering200910250ndash8

[175] Amutha KB Murugesan AG Biological hydrogen production by the algalbiomass Chlorella vulgaris MSU 01 strain isolated from pond sedimentBioresource Technology 2011102194ndash9

[176] Ji CF Legrand J Pruvost J Chen ZA Zhang W Characterization of hydrogenproduction by Platymonas subcordiformis in torus photobioreactor Interna-tional Journal of Hydrogen Energy 2010357200ndash6

[177] Dickson DJ Page CJ Ely RL Photobiological hydrogen production fromSynechocystis sp PCC 6803 encapsulated in silica sol gel InternationalJournal of Hydrogen Energy 200934204ndash15

[178] Maneeruttanarungroj C Lindblad P Incharoensakdi A A newly isolated greenalga Tetraspora sp CU2551 from Thailand with efficient hydrogen produc-tion International Journal of Hydrogen Energy 20103513193ndash9

[179] Choi SP Nguyen MT Sim SJ Enzymatic pretreatment of Chlamydomonasreinhardtii biomass for ethanol production Bioresource Technology20101015330ndash6

[180] Nguyen MT Choi SP Lee J Lee JH Sim SJ Hydrothermal acid pretreatment ofChlamydomonas reinhardtii biomass for ethanol production Journal ofMicrobial Biotechnology 200919161ndash6

[181] Hirano A Ueda R Hirayama S Ogushi Y CO2 fixation and ethanol productionwith microalgal photosynthesis and intracellular anaerobic fermentationEnergy 199722137ndash42

[182] Lee S Oh Y Kim D Kwon D Lee C Lee J Converting carbohydrates extractedfrom marine algae into ethanol using various ethanolic Escherichia colistrains Applied Biochemistry and Biotechnology 2011164878ndash88

[183] Kim JK Um BH Kim TH Bioethanol production from micro-algae Schizocy-trium sp using hydrothermal treatment and biological conversion KoreanJournal of Chemical Engineering 201229209ndash14

[184] Ferreira AF Marques AC Batista AP Marques PASS Gouveia L Silva CMBiological hydrogen production by Anabaena spmdashyield energy and CO2

analysis including fermentative biomass recovery International Journal ofHydrogen Energy 201237179ndash90

[185] Ike A Toda N Hirata K Miyamoto K Hydrogen photoproduction from CO2-fixing microalgal biomass application of lactic acid fermentation by Lacto-bacillus amylovorus Journal of Fermentation and Bioengineering 199784428ndash33

[186] Kawaguchi H Hashimoto K Hirata K Miyamoto K H2 production from algalbiomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillusamylovorus Journal of Bioscience and Bioengineering 200191277ndash82

[187] Miyamoto K Ohta S Nawa Y Mori Y Miura Y Hydrogen production by amixed culture of a green alga Chlamydomonas reinhardtii and a

photosynthetic bacterium Rhodospirillum rubrum Agricultural and BiologicalChemistry 1987511319ndash24

[188] Zhiman Y Guo R Xu X Fan X Luo S Fermentative hydrogen production fromlipid extracted microalgal biomass residues Applied Energy 2011883468ndash72

[189] Teplyakov VV Gassanova LG Sostina EG X Slepova EV Modigell MNetrusov AI Lab-scale bioreactor integrated with active membrane systemfor hydrogen production experience and prospects International Journal ofHydrogen Energy 2002271149ndash55

[190] Xue F Miao J Zhang X Tan TA New strategy for lipid production by mixcultivation of Spirulina platensis and Rhodotorula glutinis Applied Biochem-istry and Biotechnology 2010160498ndash503

[191] Lai JQ Hu ZL Wang PW Yang Z Enzymatic production of microalgalbiodiesel in ionic liquid [BMIm] [PF6] Fuel 201295329ndash33

[192] Ehimen EA Sun ZF Carrington CG Birch EJ Rye JJE Anaerobic digestion ofmicroalgae residues resulting from the biodiesel production process AppliedEnergy 2011883454ndash63

[193] Samson R LeDuy A Biogas production from anaerobic digestion of Spirulinamaxima algal biomass Biotechnology and Bioengineering 1982241919ndash24

[194] Yen HW Brune DE Anaerobic co-digestion of algal sludge and waste paper toproduce methane Bioresource Technology 200798130ndash4

[195] Sialve B Bernet N Bernard O Anaerobic digestion of microalgae as anecessary step to make microalgal biodiesel sustainable BiotechnologyAdvances 200927409ndash16

[196] Blonskaja V Menert A Vilu R Use of two-stage anaerobic treatment fordistillery waste Advances in Environmental Research 20037671ndash8

[197] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[198] Web of Science Available at langhttpappsisiknowledgecomrang[199] Scott SA Davey MP Dennis JS Horst I Howe CJ Lea-Smith DJ et al Biodiesel

from algae challenges and prospects Current Opinion in Biotechnology201021277ndash86

[200] Cooney M Young G Nagle N Extraction of bio-oils from microalgaeSeparation and Purification Reviews 200938291ndash325

[201] Sanchez OJ Cardona CA Trends in biotechnological production of fuelethanol from different feedstocks Bioresource Technology 2008995270ndash95

[202] Oncel S Sabankay M Microalgal biohydrogen production considering lightenergy and mixing time as the two key features for scale-up BioresourceTechnology 2012121228ndash34

[203] Giannelli L Torzillo G Hydrogen production with the microalga Chlamydo-monas reinhardtii grown in a compact tubular photobioreactor immersed in ascattering light nanoparticle suspension International Journal of HydrogenEnergy 20123716951ndash61

[204] Pyo D Kim T Yoo J Efficient extraction of bioethanol from freshwatercyanobacteria using supercritical fluid pretreatment Bulletin of the KoreanChemical Society 201334379ndash83

[205] Miranda JR Passarinho PC Gouveia L Bioethanol production from Scene-desmus obliquus sugars the influence of photobioreactors and cultureconditions on biomass production Applied Microbiology and Biotechnology201296555ndash64

[206] Efremenko EN Nikolskaya AB Lyagin IV Senko OV Makhlis TA Stepanov NAet al Production of biofuels from pretreated microalgae biomass byanaerobic fermentation with immobilized Clostridium acetobutylicum cellsBioresource Technology 2012114342ndash8

[207] Liu CH Chang CY Cheng CL Lee DY Chang JS Fermentative hydrogenproduction by Clostridium butyricum CGS5 using carbohydrate-rich micro-algal biomass as feedstock International Journal of Hydrogen Energy20123715458ndash64

[208] Ho KL Lee DJ Suc A Chang JS Biohydrogen from lignocellulosic feedstock viaone-step process International Journal of Hydrogen Energy 20133715569ndash74

[209] Dipasquale L DIppolito G Gallo C Vella FM Gambacorta A Picariello G et alHydrogen production by the thermophilic eubacterium Thermotoga neapo-litana from storage polysaccharides of the CO2-fixing diatom Thalassiosiraweissflogii International Journal of Hydrogen Energy 20123712250ndash7

[210] Inglesby AE Fisher AC Enhanced methane yields from anaerobic digestion ofArthrospira maxima biomass in an advanced flow-through reactor with anintegrated recirculation loop microbial fuel cell Energy amp EnvironmentalScience 201257996ndash8006

[211] Zamalloa C Vrieze JD Boon N Verstraete W Anaerobic digestibility ofmarine microalgae Phaeodactylum tricornutum in a lab-scale anaerobicmembrane bioreactor Applied Microbiology and Biotechnology 201293859ndash69

[212] Keymer P Ruffell I Pratt S Lant P High pressure thermal hydrolysis as pre-treatment to increase the methane yield during anaerobic digestion ofmicroalgae Bioresource Technology 2013131128ndash33

[213] Fernandez CG Sialve B Bernet N Steyer JP Comparison of ultrasound andthermal pretreatment of Scenedesmus biomass on methane productionBioresource Technology 2012110610ndash6

[214] Fernandez CG Sialve B Bernet N Steyer JP Thermal pretreatment to improvemethane production of Scenedesmus biomass Biomass amp Bioenergy201240105ndash11

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References
Page 24: Renewable and Sustainable Energy Reviews · Available online 19 June 2013 Keywords: Microalgae Biofuels Biodiesel Biohydrogen Bioethanol Biomethane abstract One of the most important

SS Oncel Renewable and Sustainable Energy Reviews 26 (2013) 241ndash264264

[215] Molina Grima E Belarbi EH Acien Fernandez FG Robles Medina A Chisti YRecovery of microalgal biomass and metabolites process options andeconomics Biotechnology Advances 200320491ndash515

[216] Lundquist TJ Woertz IC Quinn NWT Benemann JR A realistic technologyand engineering assessment of algae biofuel production Energy BiosciencesInstitute University of California 153

[217] Davis R Aden A Pienkos PT Techno-economic analysis of autotrophicmicroalgae for fuel production Applied Energy 2011883524ndash31

[218] Colin M Beal CM Hebner RE Webber ME Ruoff RS Seibert AF et alComprehensive evaluation of algal biofuel production experimental andtarget results Energies 201251943ndash81

[219] Delrue F Setier PA Sahut C Cournac L Roubaud A Peltier G et al Aneconomic sustainability and energetic model of biodiesel production frommicroalgae Bioresource Technology 2012111191ndash200

[220] Sing SF Isdepsky A Borowitzka MA Moheimani NR Production of biofuelsfrom microalgae Mitigation and Adaptation Strategies for Global Change20131847ndash72

[221] Rawat I Ranjith Kumar R Mutanda T Bux F Biodiesel from microalgae acritical evaluation from laboratory to large scale production Applied Energy2013103444ndash67

[222] Daroch M Geng S Guangyi Wang G Recent advances in liquid biofuelproduction from algal feedstocks Applied Energy 20131021371ndash81

[223] Jones CS Mayfield SP Algae biofuels versatility for the future of bioenergyCurrent Opinion in Biotechnology 201223346ndash51

[224] Kirrolia A Bishnoi NR Singh R Microalgae as a boon for sustainable energyproduction and its future research and development aspects Renewable ampSustainable Energy Reviews 201320642ndash56

[225] Rosenberg JN Oyler GA Wilkinson L Betenbaugh MJ A green light forengineered algae redirecting metabolism to fuel a biotechnology revolutionCurrent Opinion in Biotechnology 200819430ndash6

[226] langhttpwwwindexmundicomcommoditiesrang[227] Noureddini H Teoh BC Clements LD Densities of vegetable oils and fatty

acids Journal of the American Oil Chemists Society 1992691184ndash8[228] Amaro HM Macedo AC Malcata FX Review microalgae an alternative as

sustainable source of biofuels Energy 201244158ndash66[229] Joyce Tait et al Biofuels ethical issues a guide to the report Nuffield Council

on Bioethics 2011 16 pp[230] Buyx A Tait J Ethical framework for biofuels Science 2011332540ndash1[231] McGraw L The Ethics of Adoption and Development of Algae-based biofuels

Prepared under the outline framework of WG9 in the Ethics of Climate Changein Asia and the Pacific (ECCAP) Project RUSHSAP UNESCO 2009 83 pp

[232] Gallezot P Catalytic conversion of biomass challenges and issues Chem-SusChem 20081734ndash7

[233] Thompson PB Agricultural biofuels two ethical ıssues NABC report 200820 p 145ndash55

  • Microalgae for a macroenergy world
    • Introduction
    • Biofuels from microalgae
      • Biodiesel
      • Biohydrogen
      • Bioethanol
      • Biomethane
      • Integrated processes
      • Light to fuel
      • Future prospects
        • Economy
        • Ethical issues
        • Conclusions
        • References