Bioresource Technology 135 (2013) 182–190

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Bioresource Technology

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Potentials of macroalgae as feedstocks for biorefinery

Kyung A Jung a, Seong-Rin Lim b,⇑, Yoori Kim a, Jong Moon Park a,c,⇑a Advanced Environmental Biotechnology Research Center, School of Environmental Science and Engineering, POSTECH, 77 Cheongam-ro, Nam-gu, Pohang 790-784, South Koreab Department of Environmental Engineering, Kangwon National University, 1 Kangwondaehak-gil, Chuncheon 200-701, South Koreac Department of Chemical Engineering, Division of Advanced Nuclear Engineering, POSTECH, 77 Cheongam-ro, Nam-gu, Pohang 790-784, South Korea

h i g h l i g h t s

" This review focuses on the potential of macroalgae as a biorefinery feedstock." Their basic information and background knowledge are summarized." Their production status and carbohydrate compositions are investigated." Up-to-date macroalgae-based biorefinery technology and research are examined." Macroalgae could be utilized as a new promising biomass for low-carbon economy.

a r t i c l e i n f o

Article history:Available online 17 October 2012

Keywords:BioenergyBiorefineryBiomaterialsMacroalgaeSeaweed

0960-8524/$ - see front matter � 2012 Elsevier Ltd. Ahttp://dx.doi.org/10.1016/j.biortech.2012.10.025

⇑ Corresponding authors. Address: Department ofKangwon National University, 1 Kangwondaehak-gilKorea. Tel.: +82 33 250 6358; fax: +82 33 254 63572275; fax: +82 54 279 2699 (J.M. Park).

E-mail addresses: srlim@kangwon.ac.kr (S.-R. LimPark).

a b s t r a c t

Macroalgae, so-called seaweeds, have recently attracted attention as a possible feedstock for biorefinery.Since macroalgae contain various carbohydrates (which are distinctively different from those of terres-trial biomasses), thorough assessments of macroalgae-based refinery are essential to determine whetherapplying terrestrial-based technologies to macroalgae or developing completely new technologies is fea-sible. This comprehensive review was performed to show the potentials of macroalgae as biorefineryfeedstocks. Their basic background information was introduced: taxonomical classification, habitat envi-ronment, and carbon reserve capacity. Their global production status showed that macroalgae can bemass-cultivated with currently available farming technology. Their various carbohydrate compositionsimplied that new microorganisms are needed to effectively saccharify macroalgal biomass. Up-to-datemacroalgae conversion technologies for biochemicals and biofuels showed that molecular bioengineeringwould contribute to the success of macroalgae-based biorefinery. It was concluded that more research isrequired for the utilization of macroalgae as a new promising biomass for low-carbon economy.

� 2012 Elsevier Ltd. All rights reserved.

1. Introduction

Over the last decades, the world has been facing crucial eco-nomic and environmental issues such as fossil fuels depletionand climate change. These issues have led to the expansion of Re-search and Developments (R&D) on alternative energy with highrenewability and sustainability. As a direction of the R&D, biorefin-ery has been spotlighted as a potential solution to escape from thefossil-based economy (Ragauskas et al., 2006). Biorefinery is de-fined as sustainable processing that can convert biomass into var-ious marketable products and energy (IEA, 2009). Thus, biorefinery

ll rights reserved.

Environmental Engineering,, Chuncheon 200-701, South(S.-R. Lim), tel.: +82 54 279

), jmpark@postech.ac.kr (J.M.

should take into account the sustainability of final products. Thisimplies that biorefinery products should be produced withoutimpacting our economy and ecosystems from the life cycle per-spective (Fargione et al., 2008; IEA, 2009; Ragauskas et al., 2006).

Since biorefinery has utilized mainly crop biomass to produceliquid biofuels (e.g. bioethanol and biodiesel), that biorefineryhas significantly affected the world economy due to the competi-tion for energy and food. World production of bioethanol reachedover 51000 million liters in 2007 (RFA, 2008), and 70% of ethanolwas produced mainly from corn and sugarcane in the United Statesand Brazil, respectively (Sánchez and Cardona, 2008). Althoughbioethanol can be produced from lignocellulosic biomass as well,at present crops are regarded as the best energy resources due totheir high ethanol yield and well-established fermentation tech-nology. Consequently, this has induced the competition for energyand food resources in the global market (Sánchez and Cardona,2008). This situation also has occurred with biodiesel because itis produced from food resources such as soybean, palm oil,

K.A Jung et al. / Bioresource Technology 135 (2013) 182–190 183

rapeseed, and sunflower (Atabani et al., 2012). Due to surging foodcost from the competition, global economies have become unsta-ble; in 2006, global food stocks of major grains such as rice, wheat,and corn were at their lowest for the past 20 years (Heady and Fan,2008).

In environmental aspects, terrestrial biomass-based biorefinerycan rather exacerbate climate change when taking into accountthe life cycle of its final products. Fargione et al. (2008) andDominguez-Faus et al. (2009) reported that direct and indirect landuse change for energy crop cultivation induces a significantly high car-bon debt and high water consumption. Although many researchershave been trying to utilize lignocellulosic biomass that is not usedfor food, this biomass can still incur the same environmental con-sequences associated with land use and water consumption(Dominguez-Faus et al., 2009; Fargione et al., 2008). Thus, terres-trial biomass-based biorefinery seems not to be sustainable atpresent due to environmental as well as economic impacts.

Marine macroalgae, so-called seaweeds, have the high poten-tials to fully and partly displace terrestrial biomass and producesustainable bioenergy and biomaterials. Macroalgae do not needland and freshwater for their cultivation (Lobban et al., 1985). Mac-roalgae can convert solar energy into chemical energy with higherphotosynthetic efficiency (6–8%) than terrestrial biomass (1.8–2.2%) (FAO, 1997). Also, macroalgae have a lower risk for the com-petition for food and energy than other energy crops like corn andwheat as seaweed markets are mainly in a few East Asia countrieswhere seaweed is used for food, hydrocolloids, fertilizer, and ani-mal feed (Bixler and Porse, 2011; McHugh, 2003). Despite the envi-ronmental and economic merits of macroalgae, many challengesexist as macroalgae have unique carbohydrates, which are distinc-tively different from those of terrestrial biomass (Roesijadi et al.,2010; Sze, 1993). Due to the carbohydrate difference, terrestrialbiomass-based technology cannot be directly applied to macroal-gal biomass. Therefore, it is imperative to thoroughly review theaccumulated knowledge and information on macroalgae-basedbiorefinery.

The objective of this review is to comprehensively provide up-to-date knowledge and information on macroalgae-based biorefin-ery to show the potentials of macroalgal biomass as a feedstock forbiorefinery. Although ongoing researches on macroalgal biofuels inboth academia and industry are at infancy, interests in macroal-gae-based biorefinery continue to increase because of the necessityto resolve environmental and economic drawbacks of terrestrialbiomass-based biorefinery. This recently leads to the publicationof many research papers on macroalgal biomass and biorefineryapplications. This review first deals with basic backgrounds onmacroalgae: taxonomical classification, habitat environment, andcarbon reserve capacity. To examine a feedstock supply potentialof macroalgae, their global mass-cultivation status and carbohy-drate compositions are investigated. We also examine and discussthe macroalgae-based technology and research developed to con-vert various macroalgal carbohydrates to biomaterials and bioen-ergy. This review can help terrestrial biomass-orientedresearchers understand macroalgae as a promising new biomassfor a low-carbon economy.

2. Macroalgae backgrounds

2.1. Taxonomical classification

Macroalgae are multicellular photosynthetic organisms and be-long to the lower plants, consisting of a leaf-like thallus instead ofroots, stems, and leaves (Lobban et al., 1985). Macroalgae are clas-sified as green, red, and brown algae, according to the thallus colorderived from natural pigments and chlorophylls (Sze, 1993).

Green algae belong to phylum Chlorophyta, which has the sameratio of chlorophyll a to b as land plants (Lobban and Wynne,1981). Lewis and McCourt (2004) have addressed that higher greenplants (particularly, herbaceous plant) had evolved from green al-gae. Although this is still controversial, there is no doubt that bio-chemical compositions of green algae are similar to land plants.There are about 4500 species of green algae including 3050 speciesof freshwater-favorable algae (class Trebouxiophyceae and Chloro-phyceae) and 1500 species of seawater-favorable algae (classBryopsidophyceae, Dasycladophyceae, Siphoncladophyceae, and Ulvo-phyceae) (Guiry, 2012).

Red algae are all included in a single class (i.e., Rhodophyceae)consisting of two subclasses: Florideophycidae and Bangiophycidae.The red color is derived from chlorophyll a, phycoerythrin andphycocyanin (Lobban and Wynne, 1981; Sze, 1993). There are4000–6000 species of red algae in over 600 genera, and most ofthem exist in tropical marine environments (Yu et al., 2002).

Brown algae are classified as Phaeophyceae under phylumChrysophyta. Their principal photosynthetic pigments are chloro-phyll a and c, b-carotene, and other xanthophylls (Sze, 1993). Thereexist 1500–2000 species (Hoek et al., 1995).

2.2. Habitat environment

The pigment, growth, and chemical composition of macroalgaeare significantly affected by their habitat conditions such as light,temperature, salinity, nutrient, pollution, and even water motion,particularly depending on their taxonomical classes and specieslike Porphyra, Gelidium, Laminaria, Sargassum, Ulva and Enteromor-pha spp. (Lobban et al., 1985). Among the conditions, light is themost principal contributor. Thus, the classes of macroalgae are ver-tically distributed from the upper zone (close to the sea surface) tothe lower sublittoral zone (Lobban et al., 1985). This is becausemacroalgae have their respective pigments, which absorb selec-tively the light with specific wavelengths (Guiry, 2012). For in-stance, while most macroalgae live in the littoral zone nearcoastal line, some red algae like Gelidium sp. inhabit the deep sea(over 25 m below the surface) where sunlight availability is limited(Santelices, 1991). Gelidium sp. has phycoerythrin and phycocyaninpigments, which can efficiently absorb light with wavelengths ofphotosynthetically active radiation (PAR) that can penetrate sea-water to the deep zone (Santelices, 1991). As such, the habitatenvironment affects growth rates, size, weight, and chemical com-position (Adams et al., 2011).

2.3. Carbon reserve capacity

Macroalgae are photoauxotrophic and thus produce and storeorganic carbons (i.e., carbon sources for biorefinery) by utilizingeither CO2 or HCO3

� (Gao and McKinley, 1994). Most macroalgaedirectly uptake HCO3

� rather than CO2 for their growth becausethe diffusion rate of CO2 is extremely slow in seawater (Lobbanet al., 1985). However, a few macroalgae can utilize CO2 as a directsubstrate or accelerate the inter-conversion between CO2 andHCO3

� by using enzymes such as RuBP carboxylase and carbonicanhydrase (Lobban et al., 1985).

Due to the high photosynthetic ability of macroalgae, they havethe potential to generate and store sufficient carbon resourcesneeded for biorefinery. Table 1 shows photosynthetic rates of mac-roalgae. The photosynthetic rates highly vary depending on theirspecies (even in the same group). Note that Enteromorpha (greenalga) and Porphyra (red alga) have the highest photosynthetic rates,which are 1–2 orders of magnitude higher than those of brown al-gae. It should also be mentioned that macroalgae have higher pro-ductivity rates than terrestrial biomass such as corn andswitchgrass (Chung et al., 2011). Chung et al. (2011) estimated that

Table 1Photosynthetic rates of macroalgaea.

Species Photosynthetic rateb (lmol CO2/h)

Green algaeAcrosiphonia centralis 468 g dry�1

Cladophora rupestris 30.5 g dry�1

Codium fragile 68.3 g dry�1

Enteromorpha sp. 1786 g wet�1

Monostroma grevillei 1466 g dry�1

Ulva sp. 48.7 g dry�1

Red algaeAsparagopsis taxiformis 174 g dry�1

Chondrus crispus 21.2 g dry�1

Delesseria sanguinea 37.9 g dry�1

Gracilaria sp. 85 g wet�1

Iridaea cordata 29.4 g dry�1

Porphyra sp. 1808.7 g dry�1

Brown algaeAlaria marginata 109.3 g dry�1

Cymathere triplicata 58.5 g dry�1

Dictyopteris sp. 221 g dry�1

Fucus sp. 561 g dry�1

Laminaria sp. 124 g dry�1

Macrocystis sp. 171.8 g dry�1

Sargassum sp. 415 g dry�1

a Adjusted from Gao and McKinley (1994), Lobban and Wynne (1981).b Estimated in lmol CO2/h on the basis of dry weight (g dry�1) or wet weight

(g wet�1).

184 K.A Jung et al. / Bioresource Technology 135 (2013) 182–190

macroalgae cultivation along coastlines could sequestrate about 1billion tons of carbon annually. Muraoka (2004) reported that in Ja-pan about 32000 tons of carbon can be annually absorbed by mass-cultivated seaweeds such as Laminaria, Undaria, Hizikia, Gelidium,and Porphyra spp.

3. Mass-cultivation of macroalgae

Macroalgae are mass-cultivated based on current farming tech-nology. Although only a dozen of algae are commercially cultivatedamong over 20000 species reported worldwide (Critchley et al.,1998), the amount of macroalgae mass-cultivated in the worldhas continuously increased over the last 10 years at an average of10% (Fig. 1) (FAO, 2012a). Brown and red algae were cultivatedmore than green algae. It is noted that the red algae productiondramatically increased and the brown algae production attained

Fig. 1. World production of farmed macroalgae fro

to 15.8 million wet tons, which were harvested from wild habitatsand aquaculture farms in 2010 (note that most of them were mass-cultivated in farms) (FAO, 2012a). As shown in Table 2, the amountof the mass-cultivated macroalgae is four and six orders of magni-tude greater than for the microalgae and lignocellulosic biomass,respectively, even though the macroalgae is two orders of magni-tude less than the energy crops. This implies that with currentfarming technology, macroalgae can be more mass-cultivated tosufficiently supply feedstocks for biorefinery.

At present the most promising macroalgae species for biorefin-ery feedstock are Laminaria japonica, Eucheuma spp., Kappaphycusalvarezii, Undaria pinnatifida, and Gracilaria verrucosa (Table 2).For brown algae, only two species, L. japonica and U. pinnatifida, ac-count for over 40% of the total. For red algae, Eucheuma, Kappaphy-cus and Gracilaria spp. account for about 40%. In contrast, theproduction amount of green algae is negligible. Considering cur-rent mass-cultivation technology and market demand, macroal-gae-based refinery technology needs to be focused on utilizingbrown and red algae rather than green algae.

To increase the amount of macroalgal biomass for biorefineryglobally, international cooperation would be necessary to dissem-inate and improve the farming technology and experience of theEast Asian countries (i.e., China, Korea, Japan, Indonesia, and thePhilippines), which are the principal macroalgae producers (FAO,2012a). These countries accounted for 95% of the world’s supplyin 2010. Major species cultivated in the countries are differentdue to habitat conditions such as climate. For L. japonica and U. pin-natifida, China and Korea cultivated 85% and 30% of the total worldproduction, respectively (FAO, 2012a). While Porphyra sp. was pro-duced primarily in Japan, other red algae were cultivated mainly inIndonesia and the Philippines (Chung et al., 2011; FAO, 2012a). Dueto their farming technology and experience built up over decades,the East Asian countries would have an important role in increas-ing the amount of globally produced macroalgae for biorefineryfeedstock.

4. Chemical compositions of macroalgae

Since the biorefinery process and performance are affected bychemical compositions of feedstocks, researchers need to under-stand what types and contents of chemical resources are availablein macroalgal biomass. For instance, information on the content ofsix- and five-carbon sugars is a prerequisite to determine an

m 2001 to 2010. Adjusted from FAO (2012a).

Table 2World production of macroalgae, microalgae, energy crops, and lignocellulosicbiomass.

Species Group (or phylum) Production % of total

Macroalgaea

Laminaria japonica Brown algae 5,146,883 32.61Eucheuma spp. Red algae 3,489,388 22.11Kappaphycus alvarezii Red algae 1,875,277 11.88Undaria pinnatifida Brown algae 1,537,339 9.74Gracilaria verrucosab Red algae 1,152,108 7.30Porphyra spp. Red algae 1,072,350 6.79Gracilaria spp.b Red algae 565,366 3.58Porphyra tenera Red algae 564,234 3.57Eucheuma denticulatum Red algae 258,612 1.64Sargassum fusiforme Brown algae 78,210 0.50Phaeophyceae Brown algae 21,747 0.14Enteromorpha clathrata Green algae 11,150 0.07Monostroma nitidum Green algae 4,531 0.03Caulerpa spp. Green algae 4,309 0.03Codium fragile Green algae 1,394 0.01Gelidium amansii Red algae 1,200 0.01Total 15,784,098 100.00

Microalgaec

Arthrospira sp. Cyanophyta 3000Chlorella sp. Chlorophyta 2000Dunaliella salina Chlorophyta 1200Haematococcus pluvialis Chlorophyta 3000

Energy cropsd

Corn 844,405,181Palm oil 45,097,422Rapeseed 59,071,197Sugar cane 1,685,444,531Soybean 261,578,498

Lignocellulosic biomasse

Corn stover 12.6Switchgrass 9.0

a Estimated in wet metric ton and adjusted from FAO (2012a).b Including macroalgae cultured in brackish water.c Estimated in dry metric ton and adjusted from Hejazi and Wijffels (2004),

Lorenz and Cysewski (2000), Pulz and Gross (2004), Ratledge (2004).d Estimated in ton and adjusted from FAO (2012b).e Estimated in dry metric ton a hectare and adjusted from Lemus et al. (2002),

Shinners and Binversie (2007).

K.A Jung et al. / Bioresource Technology 135 (2013) 182–190 185

appropriate fermentation microorganism and a process for bioeth-anol production. Also, that kind of information would be helpful tounderstand what biomaterials can be readily and economicallyobtained or converted through biorefinery.

4.1. Difference between terrestrial- and marine-biomass

Macroalgae are significantly different from terrestrial plants interms of their chemical composition, as well as physiological andmorphological features. Table 3 shows the type of principal carbo-hydrates included in marine macroalgae, microalgae, and lignocel-lulosic biomass. Macroalgae have manan, ulvan, carrageenan, agar,laminarin, mannitoal, alginate, and fucoidin (Lobban and Wynne,1981), which are not included in microalgae and lignocellulosicbiomass. Thus, the monosaccharides hydrolyzed from these carbo-hydrates and/or whole polysaccharides should be targeted to de-velop macroalgae-based biorefinery technology. Like terrestrialbiomass, macroalgae except green algae do not have the high con-tent of starch and oil (Roesijadi et al., 2010), which is differentiatedfrom microalgae (Brown, 1991). It should be noted that macroalgaealmost do not include lignin because macroalgae do not need tostand rigidly in the water (Wegeberg and Felby, 2010): lignin is aconstituent needed for the rigidity of terrestrial plants. Thus, thecell wall of macroalgae is structurally flexible. Due to their low lig-nin content, macroalgae can provide many benefits for biorefinery:no need for complex processes such as lignin removals and detox-

ification of lignin-originated inhibiting compounds (Meinita et al.,2012a). Compared to the terrestrial biomass, macroalgae have thehigh contents of water (70–90% fresh wt.) and minerals such as ali-kali metals (10–50% dry wt.) (Ross et al., 2008). In contrast, theyhad the low contents of protein (7–15% dry wt.) and lipids (1–5%dry wt.) (Jensen, 1993), whereas most microalgae have the highcontent of protein (40–60% dry wt.) and intermediate lipids (10–20% dry wt.) (Becker, 1994).

4.2. Carbohydrate composition of macroalgae

Carbohydrate compounds are abundant in macroalgae. The car-bohydrate contents of green, red, and brown algae are 25–50%, 30–60%, and 30–50% dry wt., respectively (Becker, 1994; Jensen, 1993;Ross et al., 2008). Since macroalgae have a variety of carbohydratesdepending on their species, information on their carbohydratecompositions is necessary to effectively utilize them as carbonsources for bioenergy and as chemical sources for biomaterialand bioproducts.

4.2.1. Green algaeGreen algae have polysaccharides in the form of starch (i.e., a-1,

4-glucan) and lipids but their proportions are small (1–4% forstarch; and 0–6% for lipids) (Bruton et al., 2009). Ulva and Entero-morpha sp. have water-soluble ulvan and insoluble cellulose (38–52% dry wt.) in their cell walls (Lahaye and Robic, 2007). Ulvan, adistintive feature of green algae, is composed mainly of D-glucu-ronic acid, D-xylose, L-rhamnose, and sulfate (Lobban and Wynne,1981).

4.2.2. Red algaeRed algae are different from green and brown algae in the syn-

thesis and metabolism machinery of carbohydrates. The uniquecarbohydrates for red algae are floridean starch and floridoside,which are similar to general starch, but green and brown algaedo not have those carbohydrates (Sze, 1993; Yu et al., 2002). Flor-idean starch is an a-1,4-glucosidic linked glucose homopolymerand accounts for up to 80% of the cell volume (Yu et al., 2002). Be-cause floridean starch has the property to weaken gel strength, it isremoved as an impurity in the production of agar and carrageenanby using thermophilic a-amylase treatment (Yu et al., 2002).

The major polysaccharide constituents of red algae are galac-tans such as carrageenan (up to 75% dry wt.) and agar (up to52%), which are the most commercially important polysaccharidesfor red algae (Lobban and Wynne, 1981; McHugh, 2003). Carra-geenan consists of repeating D-galactose unit and anhydrogalac-tose, which may or may not be sulfated (Lobban and Wynne,1981). Carrageenans can be readily obtained by extracting red sea-weeds or dissolving them into an aqueous solution (McHugh,2003). Purified carrageenans are generally used for forming thicksolution or gel (Lobban and Wynne, 1981). Commercial carrageen-ans have been originated from Chondrus, Gigartina, and Eucheumasp. (Vera et al., 2011). As another major constituent, agar is madeup of alternating b-D-galactose and a-L-galactose with scarce sulf-ations (Lobban and Wynne, 1981). If these galactose compoundsare highly sulfated, that agar cannot make a gel structure (Lobbanand Wynne, 1981). Agars are utilized as algal hydrocolloids in food,pharmaceutical, and biological industries (Bixler and Porse, 2011).Agar is produced from Gracilaria, Gelidium, and Pterocladia sp. bytreating them with acid/heat or alkali (McHugh, 2003).

4.2.3. Brown algaeA major polysaccharide of brown algae is alginic acid (i.e., algi-

nate), which accounts for up to 40% dry wt. as a principal materialof the cell wall (Draget et al., 2005). Alginate is composed of threedifferent uronic acids: mannuronic acid blocks, guluronic acid

Table 3Carbohydrate composition of macroalgae, microalgae, and lignocellulosic biomass.

Macroalgaea Microalgaeb Lignocellulosic biomass

Green algae Red algae Brown algae

Polysaccharide Polysaccharide Polysaccharide Starch CelluloseMannan Carrageenan Laminarin Total carbohydrate HemicelluloseUlvan Agar Mannitol Arabinose LigninStarch Cellulose Alginate FucoseCellulose Lignin Fucoidin GalactoseMonosaccharide Monosaccharide Cellulose GlucoseGlucose Glucose Monosaccharide MannoseMannose Galactose Glucose RhamnoseRhamnose Agarose Galactose RiboseXylose Fucose XyloseUronic acid XyloseGlucuronic acid Uronic acid

Mannuronic acidGuluronic acidGlucuronic acid

a Adjusted from Jang et al. (2012), Roesijadi et al. (2010), Turvey and Christison (1967), Wegeberg and Felby (2010).b Adjusted from Brown (1991).

186 K.A Jung et al. / Bioresource Technology 135 (2013) 182–190

blocks, and alternative blocks of mannuronic and guluronic units(Lobban and Wynne, 1981). Alginate tends to become gel due toits high affinity for divalent cations such as calcium, strontium,barium, and magnesium (Draget et al., 2005). Various brown algaetend to have their respective alginate structure and proportions ofmannuronic and guluronic acids in alginate (Lobban and Wynne,1981). Alginates have been used mostly in the textile (50%) andfood (30%) industries (McHugh, 2003).

As a unique polysaccharide for brown algae, they have lami-narin (i.e., b-1, 3-glucans) (Adams et al., 2011). This polysaccharideaccounts for up to 35% dry wt. of brown algae (Mautner, 1954).Their laminarin contents vary depending on seasons and waterdepth, which affect nutrient conditions for growth of macroalgae(Adams et al., 2011; Mautner, 1954). Brown algae also have fucoi-dan, which is a sulphated complex polysaccharide consisting of fu-cose and a linear backbone of sulfate monosaccharides (Holtkampet al., 2009). Fucus vesiculosus is used to produce relatively purefucoidan (Duarte et al., 2001). Fucoidan has been extensively stud-ied due to its potential in pharmaceutical applications (Li et al.,2008). In addition, brown algae have glucose and glyoxylic acidin small amounts (Mautner, 1954).

5. Biomaterials and bioproducts from macroalgae

At present, macroalgae are utilized for human food, algal hydro-colloids, therapeutic materials, fertilizer, and animal feed. Amongmacroalgae-related industries, the food industry is the largest,accounting for $5 billion worldwide on an annual basis, which is83–90% of the total seaweed industry (Roesijadi et al., 2010). Sea-weed food markets are mainly in the East Asian countries(McHugh, 2003). Macroalgae themselves are uptaken as foodingredients and converted to other products. For instance, agar isused as food ingredients, and carrageenan as food additives fordairy, meat, water-based, and pet foods (McHugh, 2003).

Besides food uses, macroalgae are utilized to produce diversebiomaterials and bioproducts in various industries. One of the prin-cipal materials is algal hydrocolloids, which accounts for $132–240million worldwide on an annual basis, and their key componentsare agar, alginate, and carrageenan (Roesijadi et al., 2010). Annualworld sales amount of seaweed hydrocolloids has increased by 6%from 1999 to 2009, and its sales amounts have almost doubled inthat period (Bixler and Porse, 2011). Since macroalgae have respec-tive characteristics for gel-forming and water-dissolving, variousmacroalgae are used for industrial uses (McHugh, 2003). Agar is

used as a laxative in the pharmaceutical industry and as a chemicalto test the presence of bacteria (McHugh, 2003). Carrageenan isutilized as an essential ingredient in toothpaste (McHugh, 2003),even though this market is not large. Alginate is used in onlynon-food industries such as textile printing, immobilized biocata-lyst, pharmaceutical tablet disintegrant, medical fiber, weldingrod, and paper industries (Bixler and Porse, 2011; Kraan, 2010;Roesijadi et al., 2010).

Several polysaccharides and oligosaccharides derived frommacroalgae are used for therapeutic applications due to their bio-activity (Jiao et al., 2011; Li et al., 2008; Vera et al., 2011). For in-stance, the saccharides are fucodidan and fucan from brownalgae; sulfated galactan and ulvan-like sulfated polysaccharidefrom green algae; and sulfated polysaccharides such as carra-geenan and galactan from red algae. These substances were recog-nized to have antithrombotic, antiviral, immuno-inflammatory,antilipidemic, and antioxidant activities (Jiao et al., 2011). Veraet al. (2011) reported that ulvan, alginate, fucan, laminarin, andcarrageenan and their derived oligosaccharides could increasethe immune ability of terrestrial plants against pathogens by acti-vating signal pathways in the plants.

In addition to the aforementioned biomaterials, many effortsare being taken to develop the precursors of biomaterial buildingblocks and fermentation products from macroalgae. The precursorsare derived as main products and byproducts from biorefinery pro-cesses using physiochemical treatment and microbial fermentation(Chang et al., 2010). Kraan (2010) and Chang et al. (2010) have re-ported some possible fermentation products and high-valuebyproducts from macroalgae. The yield and the selectivity offermentation products depend largely on reaction conditions(Gunaseelan, 1997; Veeken et al., 2000), which are determinedby taking into account economic viability of building block prod-ucts. Volatile fatty acids (VFAs) such as acetic, propionic, lactic,and butyric acids can be produced from macroalgae by usinganaerobic digestion. Chang et al. (2010) have suggested a novelplatform using these VFAs to produce chemicals and fuels. Inprevious studies, anaerobic digestion has been applied to generatelactic acid as well as methane from macroalgal biomass (Guptaet al., 2011). Due to the low lignin content of macroalgae, valuableVFAs could be efficiently produced by anaerobic digestion.

Other bioproducts derived from macroalgae are amino acids.Lammens et al. (2012) have evaluated the availability of protein-derived amino acids from byproducts of macroalgal biorefinerybecause glutamic acid can be a source of valuable bio-basedchemicals, i.e., as N-methylpyrrolidone, N-vinylpyrrolidone, and

K.A Jung et al. / Bioresource Technology 135 (2013) 182–190 187

acrylonitrile. Although macroalgae have a wide range of proteincontents depending on their species, the average protein propor-tion (20%) of macroalgae is higher than for other crop residues suchas corn stover, wheat straw, and sugarcane leafs (Lammens et al.,2012).

6. Bioenergy from macroalgae

6.1. Biogas

Anaerobic digestion can be applied to produce biogas, particu-larly methane, from various macroalgae (Gupta et al., 2011).Gunaseelan (1997) has compared digestion characteristics of sev-eral land- and water-based biomass. According to this work, themacroalgae (0.31–0.48 m3 CH4 kg�1 volatile solid) exhibited highermethane production rates than the land-based biomass (0.34–0.42 m3 CH4 kg�1 for grass, and 0.32–0.42 m3 CH4 kg�1 for wood),and kelp was only biomass that did not need pretreatment, be-cause of no existence of lignin. It should be mentioned that theanaerobic digestion performance is affected by the species andthe composition of macroalgae, depending on seasons, geography,and so on (Costa et al., 2012). Methane production rate can be im-proved by co-digesting macroalgae (Ulva sp.) with manure andwaste activated sludge (Costa et al., 2012). While biogas produc-tion from macroalgae is more technically-viable than for otherfuels, that biogas production is not yet economically-feasible dueto the high cost of macroalgae feedstocks, which needs to be re-duced by 75% of the present level (Roesijadi et al., 2010).

6.2. Bioethanol

Bioethanol can be fermented from all kinds of macroalgae byconverting their polysaccharides to simple sugars and by employ-ing appropriate microorganisms. Since macroalgae have variouscarbohydrates such as starch, cellulose, laminarin, mannitol, andagar, carbohydrate conversion to sugars and the choice of appro-priate microorganisms are pivotal for successful bioethanol fer-mentation; however, those researches are now at the early stage.

Brown algae are a principal feedstock for bioethanol productionbecause they have high carbohydrate contents and can be readilymass-cultivated with current farming technology. Among theircarbohydrates, mannitol and laminaran (for Laminaria sp., 25%and 30% dry wt., respectively (Horn et al., 2000a)) are the mostreadily utilized by certain microorganisms (Horn et al., 2000a,b).Horn et al. (2000a,b) have shown that mannitol and laminaran ex-tracts from L. hyperborea can be fermented to produce bioethanol.They have also examined the ethanol fermentation performancefor brown algae extracts by applying various bacteria and yeasts.Bacterium Zymobacter palmae converted only mannitol to ethanoldue to its lack of laminarase activity, whereas two yeast strainsKluyveromyces marxianus and Pacchysolen tannophilus fermentedlaminaran but not manitol. Only yeast Pichia angophorae has simul-taneously utilized both mannitol and laminaran to produce etha-nol. This yeast achieved the highest yield of 0.43 g ethanolg substrate�1.

Many attempts have been taken to utilize various carbohy-drates in macroalgal biomass by using physicochemical hydrolysis,as in the saccharification of lignocellulosic biomass. Dilute-acidhydrolysis is a typical physicochemical method to treat raw macro-algal biomass with 0.3–0.9 N H2SO4 at 100–140 �C (Meinita et al.,2012b; Park et al., 2012). In the acid hydrolysis, reaction parame-ters such as acid concentration and hydrolysis time affect the totalyields of reducing sugars and ethanol production: optimum condi-tions need to be determined to maximize concentrations of mono-sugars and ethanol (Meinita et al., 2012b).

Besides chemical hydrolysis, enzymatic hydrolysis is anothergeneral and mild approach to saccharify macroalgal biomass. How-ever, its procedures for high ethanol productivity have been under-developed because the enzyme activity is specific to the type ofpolysaccharides while even a single species of macroalgae consistsof more than one type of polysaccharide complexes (Choi et al.,2009). Many studies have carried out macroalgae hydrolyses byusing cellulase and cellobiase as for lignocellulosic biomass (Geet al., 2011; Yanagisawa et al., 2011) as well as commercial enzymecomplexes (Choi et al., 2009). A few studies have applied macroal-gae-specific enzymes such as laminarinase and agarase to sacchar-ify macroalgae; however, these enzymes showed low hydrolysisefficiency. Thus, their treatment needs additional pretreatment ormulti-enzyme complexes (Adams et al., 2011).

Chemical and enzymatic hydrolyses have been combined tomore effectively obtain mono-sugars from macroalgae (Adamset al., 2011; Ge et al., 2011; Jang et al., 2012). A thermal acid hydro-lysis and an enzyme treatment were applied to Saccharina sp. andLaminaria sp. (brown algae) to recover potentially fermentablereducing sugars such as D-mannuronate, L-guluronate, D-glucose,L-fucose, D-galactose, D-xylose, and L-glucuronate (Ge et al., 2011;Jang et al., 2012). Gelidium amansii and Kappaphycus alvarezii (redalgae) were more readily fermented than brown algae by usingchemical and enzymatic hydrolyses (Park et al., 2012).

More elaborate research has been performed to investigate theoptimal pretreatment with respect to the carbohydrate character-istics of macroalgae species. Yanagisawa et al. (2011) have sug-gested tailor-made saccharification methods to increasebioethanol yields for green, red, and brown algae. For G. elegans(red alga), a combined saccharification process consisting of acidand enzyme hydrolyses was used to convert the original polysac-charides (i.e., galactan and glucan) to galactose and glucose(Lobban and Wynne, 1981). This red algae-specific saccharificationled to an increase in the ethanol concentration (5.5% vol., or 0.44 gethanol g glucose�1), which is higher than the economically feasi-ble concentration (4–5%) for distillation. For Ulva pertusa and Alariacrassifolia (green and brown algae, respectively), an enzymatichydrolysis was enough to saccharify because glucan, a singlepolysaccharide in the two seaweeds, can be hydrolyzed to glucoseby the enzyme (Yanagisawa et al., 2011).

Pretreatment for saccharification can inhibit microbial fermen-tation, and thus detoxicification research is required to effectivelyutilize macroalgal biomass. Heat and pH pretreatments have beenfound to rather lower bioethanol yields for a brown alga (Saccha-rina latissima) (Adams et al., 2009). Although heat treatment isused to solubilize laminaran, that heat can generate inhibitorycompounds. Also, acid treatment has caused the ethanol yield forS. latissima to decrease by 40–47%, probably due to cell disruptionand salt inhibition (Adams et al., 2009). Representative inhibitorycompounds generated in the acid hydrolysis condition (even in di-lute acid solutions) are furfural, 5-hydroxymethylfurfural (HMF),levulinic acid, and caffeic acid (Meinita et al., 2012a). These com-pounds are derived primarily from xylose and galactose in macro-algal biomass. The inhibitors can be detoxified by applying limeand activated charcoal treatments (Meinita et al., 2012a). Anotherinhibition on microbial fermentation could be derived from themetals in macroalgae, which could be released to the broth duringpretreatment. This is because the metal contents (0.5–11% wt.) ofmacroalgae are higher than for terrestrial biomass (1–1.5% wt.)(Lee and Lee, 2012; Ross et al., 2008).

6.3. Biobutanol

Biobutanol can be produced from macroalgae through the ace-tone-butanol (AB) fermentation using solventogenic anaerobicbacteria such as Clostridium sp. (Huesemann et al., 2012).

Table 4Microorganisms and enzymes that can degrade macroalgal polysaccharides.

Species

Green algaeUlvanGram-negative marine bacterium (ulvan lyase, endo-)

Red algaeAgarAlteromonas sp. C-1(b-agarases, extra-)Bacillus sp. MK03 (b-agarases, extra-)Pseudomonas atlantica (b-agarases I, II, endo-)Thalassomonas sp. JAMB-A33 (a-agarases, intra-)Vibrio sp. JT0107 (b-agarases, extra-)CarrageenanAlteromonas fortisDelesseria sanguineaPseudoalteromonas carrageenovoraZobellia galactanivorans

Brown algaeAlginateAlginovibrio aquatilis (alginate lyases, endo-)Alteromonas sp. strain H-4 (alginate lyase, exo-)Asteromyces cruciatus (alginate lyases, endo-)Dendryphiella arenaria (alginate lyase)Marine bacterium ATCC 433367 (alginate lyases, exo-/endo-)Pseudoalteromonas elyakovii IAM 14594 (alginate lyase, exo-)Sphingomonas Strain A1 (alginate lyase, exo-)Vibrio sp. (alginate lyase)

FucoidanPecten maximus (intra-/extra- cellular)Pseudomonas atlantica (fucoidanase)Pseudoalteromonas atrea KMM3296 (fucoidanase)Pseudoalteromonas citrea (fucoidanase)Vibrio sp. (fucoidanase)

LaminarinAplysia julianaChaetomium indicum (laminarinase)Pseudoaltermonas issachenkonii KMM 3549 (laminarinase; fucoidan

hydrolase; alginase)Vibrio sp. 3 strains (laminarinase)

Adjusted from Alderkamp et al. (2007), Holtkamp et al. (2009), Reddy et al. (2008).

188 K.A Jung et al. / Bioresource Technology 135 (2013) 182–190

Clostridium sp. is capable of producing butanol, acetone, ethanol,and organic acids from various carbon substrates. However, thisbacterium did not effectively utilize some glucose-based polysac-charides (such as mannitol from brown algae), which causedslow reaction rate and low productivity of organic acids and totalsolvents (Huesemann et al., 2012).

6.4. Advanced technology for macroalgal biofuels

To commercialize macroalgae-based fuels, a priority needs to beput on identifying microorganism that can metabolize major butunique macroalgal carbohydrates. Some macroalgae-specific car-bohydrates such as alginate and ulvan are not readily metabolizedby commercially applied fermenting microorganisms such as Sac-charomyces cerevisiae (Wegeberg and Felby, 2010). To overcomethis drawback, some researchers have developed macroalgae-specific enzymes to hydrolyze macroalgal carbohydrates (Janget al., 2012). Table 4 shows microorganisms and enzymes thatcan degrade various macroalgal carbohydrates. Most of the micro-organisms were originated from marine flora and fauna. Theirenzymatic functions on macroalgae have been well reviewed inmany studies (Erasmus et al., 1997).

Once those kinds of microorganisms and enzymes have beenidentified and developed, they can be applied to the SimultaneousSaccharification and Fermentation (SSF) system (Jang et al., 2012).This SSF system has many advantages: low contamination, low ini-tial osmotic stress of fermenting microorganisms, and high energy-

efficiency. It should be noted however, that applying variousmicroorganisms to a fermentation condition as in the SSF systemcould inhibit enzyme activity and extracellular enzyme secretion(Alderkamp et al., 2007; Holtkamp et al., 2009; Reddy et al.,2008). Also, various and complex carbohydrates of macroalgaecan lead to low yield of biofuels in the SSF system (Jang et al.,2012).

Recently, advanced biotechnology has been applied to resolveaforementioned challenges in macroalgae-based biorefinery: so-called Consolidated BioProcessing (CBP) (Kim et al., 2012; Sánchezand Cardona, 2008; Wargacki et al., 2012). This CBP consists of adiverse range of genetic transformation and metabolic engineering,which are expected to provide a breakthrough in the developmentof biomass-based bioenergy technology in the next 10 years. Kimet al. (2012) have reported that S. cerevisiae was engineered to ex-press heterologous sugar transporters and thereby remove glucoserepression under the mixed sugars condition. Also, secondarysugar transporters and some metabolic genes were expressed tobypass the regulatory mechanisms of the S. cerevisiae and thusco-ferment mixed mono-sugars simultaneously. Wargacki et al.(2012) have shown that biofuel was produced directly from algi-nate by engineering secretable alginate lyases from Vibrio splendi-dus and functional alginate transport and metabolic systems intoEscherichia coli. This approach has achieved 4.7% vol. (or0.281% wt.) of ethanol yield, which surpasses the ideal ethanolyield (0.254% wt.) for macroalgae.

Besides improving microbial abilities molecular bioengineeringis required to modify the physicochemical properties of macroal-gae and make them readily utilized for biofuel production (Renn,1997). For instance, metabolic engineering could be applied to sea-weeds in order to alter their biosynthetic pathways and therebyimprove their polysaccharide composition and productivity (Renn,1997). This approach could significantly improve seaweed produc-tivity and contribute to the success of marine biorefinery. Althoughmeaningful outcomes have yet been reported due to difficulties inthe genetic manipulation of macroalgae, many efforts have beentaken to develop molecular biotechnology on macroalgae; for in-stance, gene mapping, introduction of foreign genes into seaweedcells, and promoter selection (John et al., 2011; Qin et al., 2004;Renn, 1997).

7. Conclusions

Macroalgae have the high potential as feedstocks for biorefineryto produce biomaterials and bioenergy. Macroalgae-based biore-finery is expected to dramatically develop in the near future, dueto many environmental and economic benefits. For biorefineryfeedstock supply, macroalgae can be mass-cultivated with cur-rently available farming technology. However, due to various mac-roalgal carbohydrates, more efforts should be taken to effectivelyand efficiently utilize macroalgae: identification of new microor-ganisms, technology development for genetic transformation andmetabolic engineering, and process development and optimizationfor yield enhancement. Once these technologies are established,macroalgae could significantly contribute to low-carbon economyas a most promising biomass.

Acknowledgements

This research was supported by Basic Science Research Programthrough the National Research Foundation of Korea (NRF) fundedby the Ministry of Education, Science and Technology (Grant num-bers 2011-0001108 and 2011-0008373), the Advanced BiomassR&D Center (ABC) of Korea Grant funded by the Ministry of Educa-tion, Science and Technology (ABC-2011-0028387), Marine

K.A Jung et al. / Bioresource Technology 135 (2013) 182–190 189

Biotechnology Program funded by Ministry of Land, Transport andMaritime Affairs of Korean Government, Korea and the ManpowerDevelopment Program for Marine Energy funded by Ministry ofLand, Transportation and Maritime Affairs (MLTM) of Korean gov-ernment, by WCU (World Class University) program through theNational Research Foundation of Korea funded by the Ministry ofEducation, Science and Technology (R31-30005), and by 2011 Re-search Grant from Kangwon National University.

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