Artificial Biofuels (2010)

8/12/2019 Artificial Biofuels (2010)

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Biofuels (2010) 1(6) future science group862

Review Cogdell, Brotosudarmo, Gardiner, Sanchez & Cronin

The importance of efficiency At this point there wi ll be asmall digression about efciency.Different groups of scientists quotedifferent types of efciency and this

can lead to a degree of confusion[101] . Often researchers who studythe early reactions of photosynthesisquote quantum efciency (QE). QEis dened as the percentage of thenumber of absorbed photons thatproduce the reaction. In the case ofthe light reactions of photosynthesis,the QE of charge separation in thereaction center is very nearly 100%.Biologists who study whole-plantphotosynthesis usually use a mea-

sure of efciency that is dened asthe energy of the biomass produceddivided by the total energy of thephotosynthetically active radiation(PAR, this means only the fraction

of the incident solar radiation that plants can absorb)absorbed. Physicists who study solar cells dene ef-ciency as the energy output of the cell divided by thetotal energy available from the incident solar radiationon the surface of the cell. The efciencies quoted herehave been calculated on the same basis as that used bythe physicists. Efciencies with solar cells of between 10and 20% can be readily obtained[101] . The magnitudeof these efciencies represents the extent of the challengethat articial photosynthesis must meet.

Currently, mankind consumes 4.1 1020 J per year.Nathan Lewis has calculated how much of the surfaceof the USA would need to be covered with solar energycollectors to provide for all their current energy needs,assuming an efciency of 10%[102] . The answer is 1.7%.The lower the efciency of conversion of the solar energyinto fuel, then the larger the surface area required. Any proposed solar energy conversion system must besocially acceptable. If the land area requirements are toolarge then this becomes a real problem. Current cropsused for biofuels are already competing for land withthose grown for food or promoting habitat destruction,so the advisability of doing this has been seriously ques-tioned. This controversy will get even worse should thisprocess be scaled up to the level required for the currentgeneration of biofuels to be major sources of energy. When grown under optimum conditions, the maxi-mum efciency of conversion of solar energy into totalbiomass has been estimated to be 4.6% inC3 plants and a little higher inC4 plants at 6%[5]. However, onlya fraction of this biomass can be currently convertedinto, for example, bioethanol. This results in an even

lower energy conversion efciency, so, correspond-ingly, a greater land area is needed. Current estimatesof the average efciency of conversion of solar energyinto fermentable biomass are approximately 0.3%. Touse plants at this level of efciency to produce all our

energy needs would require approximately 31% of thetotal land area of our planet[102] . The cost of producingfuels such as bioethanol must also be considered.Box 1 shows an interesting breakdown of the costs of bioetha-nol relative to that of gasoline based on data from March2006. The two points to note are the importance of thesubsidy given and the fact that bioethanol productionbecomes increasingly economically feasible as petrol(gasoline) prices rise. The largest factor determiningwhether or not bioethanol production makes economicsense is, therefore, the cost of a barrel of oil. This iscurrently a highly mobile target. Even if so-called rst-

generation bioethanol becomes economic it is an alto-gether different question to ask whether its productionis a good idea or not? However, if more of a plantsbiomass could be converted to ethanol, then both theefciency of its production would rise and its cost wouldgo down. This explains the drive to make systems thatcan transform both cellulose and lignin into ferment-able substrates. This target is the main aim of the largesolar energy research center based at the University ofCalifornia at Berkeley (CA, USA) and the University ofIllinois at Champaign-Urbana (The Energy BioscienceInstitute[103] ; IL, USA) and the Department of EnergyCenters at Oak Ridge National Laboratories (TN,USA) and the Universities of Wisconsin (WI, USA)and Michigan State (MI, USA)[104] .

Is it possible to think of using photosynthesismore efciently[5]? In order to try and answer thisquestion we need to consider what happens in thephotosynthetic process.

The essence of photosynthesisIt is possible to break down photosynthesis into foursequential, partial reactionsFigure 1 [105] . The rst reac-tion is light harvesting or light concentration. The sec-ond uses this concentrated light to separate charge acrossa membrane (in photosynthesis this is the function of thereaction centers). The third reaction involves using theaccumulated positive charges to oxidize water and thefourth uses the resultant negative charges for reductivechemistry to produce the fuel. Production of the fuelrequires a supply of sufciently reducing electrons andwater is the most accessible and abundant source forthese. The model inFigure 1 is of course a simplicationsince in the natural process reduction of carbon dioxideto carbohydrate not only involves the participation of asecond photosystem but also requires ATP. However, itdoes provide a useful conceptual framework. Clearly, if it

Key terms

Photosynthesis: The biological processfound in plants, algae and somebacteria that uses solar energy toconvert carbon dioxide intocarbohydrate.

Bioethanol: Ethanol that is produced bythe fermentation of plant sugars. Theimpure ethanol is then distilled toproduce a product that can be addedto supplement petroleum products foruse in transportation.

Articial photosynthesis: The assemblyof chemical systems, the constructionof which is inspired by biology, that arecapable of mimicking the main stagesof photosynthesis.

C3 plants: Plants such as spinach thatinitially x carbon dioxide into a3-carbon sugar, 3-phosphoglyceric acid.

C4 plants: Plants such as sugarcane thatinitially x carbon dioxide into 4-carbonacids, such as oxaloacetic acid.


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Articial photosynthesis solar fuels: current status & future prospects Review

future science group www.future-science.com 863

is possible to intervene in the photo-synthetic process early enough then,theoretically, the energy conversionefciency will be higher. The higherthe efciency, the smaller the quan-

tity of land required, and the morepotentially acceptable the solutionbecomes.

Intervening earlier in the lightreactions and substituting alterna-tives for the dark reactions is theidea behind the concept of articialphotosynthesis. The term articial photosynthesis can beconfusing since it has been used in many different ways.Often it is used when an attempt is made to mimic anysingle stage of the four shown inFigure 1 . Here, we havetried to use this term to refer to mimicking all four stages.

Is it possible to use this simplied model of photosynthesisto build robust chemical systems that can mimic naturalphotosynthetic reactions and so use solar energy more ef-ciently to make a suitable fuel? In recent years a great dealof progress has been made in understanding the struc-ture and function of the various pigment protein com-plexes that catalyze the early reactions of photosynthesis,namely the antenna complexes and the reaction centers.Readers interested in this work should consult these twoexcellent books[6,7]. In both antenna complexes and reac-tion centers the processes of energy transfer and electrontransfer are essentially temperatureindependent. In other words, thereis no molecular motion involved andthe proteins simply act as a scaffoldto set the optimum preconditionsfor the energy and electron transferreactions. The proteins do not play anactive role in these reactions over thetimescale during which they occur.This means that the x-ray crystalstructures of these pigment proteincomplexes can be used as excellentmodels on which to base the designof articial mimics. Indeed, there arenow many examples of such syntheticmolecules that can be successfullyassembled into systems capable ofabsorbing solar energy and using it todrive efcient charge separation[812] .

The real barriers to producingarticial systems capable of mim-icking the overall reactions of pho-tosynthesis are those associated withbeing able to replicate the slowerreactions of water oxidation andthe reductive synthesis of the fuel.

In both cases the x-ray crystal structures of the enzymesinvolved in these processes are known, but also, in bothcases, the proteins actively participate in the catalyticmechanisms involved. As a result, the structure of theactive sites visualized in the protein structures only pro-vides a single static view. The precise details of what goes

on in the reactions are, therefore, not clear and mim-ics, which are usually rigid, fail. In the case of photo-synthetic reduction of carbon dioxide to carbohydratethere is also a major problem with the main enzymeRUBISCO. This enzyme not only has a rather low afn-ity for carbon dioxide but also has areaction with oxygen that results inthe loss of one of the previously xedcarbon atoms. A great deal of worktrying to improve RUBISCO hasbeen carried out without signicant

Box 1. Price of corn-based ethanol versus price of gasoline.

Cost of ethanol in 10 midwestern states on March 22, 2006 (US$/gal) 2.342.50Subsidy (American Jobs Creation Act of 2004, PL. 108 357) (US$/gal) 0.51Net cost of ethanol (US$/gal) 1.831.99Energy Content (BTU/gal): Gasoline 125,000 Ethanol 76,000Gallons of ethanol per gallon gasoline equivalent 1.6Price of ethanol per gallon gasoline equivalent (US$/gal) 2.923.18Retail price of regular grade gasoline in Midwest, March 20, 2006 (US$/gal) 2.50Data from [4].

Antenna

Harvesting light

Energytransfer

Catalyticsite 2

Catalyticsite 1

Hydrogen+

methanol

H2O + HA

H+ + CO 2

O 2 + A + H+

1

3

4

Reaction center

Electron gradient

Electron transfer Electron transfer

2

Figure 1. Blueprint for the coupling of an antenna system with a reaction center that iscoupled with catalytic site 1 and catalytic site 2. Catalytic site 1 oxidizes water whereascatalytic site 2 xes carbon dioxide. The key issue is to develop modular and congurable routesto join the various components together.

Key term

RUBISCO: Ribulose 15 bis-phosphatecarboxylase/oxygenase. This is theprimary enzyme that xes carbondioxide forming carbohydrates.


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progress[13] . Producing new cata-lysts capable of xing carbon diox-ide into a suitable fuel that are ableto work at the low concentrationsof carbon dioxide present in the

atmosphere is a very severe challenge indeed.Choosing the appropriate fuelBefore discussing in more detail proposed strategies forbuilding systems capable of using solar energy to makefuel(solar fuel) , it is important to consider what fuel totry and make. This is important because it will inuencesubsequent research strategies and because in differ-ent situations different choices may be appropriate. Insome cases the answer could be hydrogen but in othersa more dense, portable liquid hydrocarbon might bepreferable. Hydrogen could be a good fuel for heating

and powering automobiles, but not for airplanes. Flyingwill require the denser liquid hydrocarbons. Choosingto make a fuel that is miscible with water introducesother problems. Methanol and ethanol might be rathereasy to make, however, a lot of energy is then needed todistil away these fuels from water to obtain them in suf-cient concentration/purity that they are combustible.Self-evidently, these cannot not be fuels of choice if toogreat an energy input is required simply to get theminto a useable form.

In the current rush to produce biofuels not enoughthought has been given to what is the best type of fuelto aim for. This is a very serious issue indeed. If biofuelsare tarred with a bad name in a similar way to geneti-cally modied organisms, then there is a danger that,even after sensible sustainable systems for making solarfuels have been developed, an alienated public opinionwill have too much opposition for them to be accepted.Now is the time to engage with the public on theseissues so that the ground is well prepared when possiblesolutions are found.

Articial photosynthesis Although it is sensible to attempt to develop plants thatcan convert solar energy into biomass/fuels with increas-ing efciency, there are large barriers that must be over-come in order to achieve this. For example, plants grownfor energy would need to be located on land either classedas marginal, where plant growth might be expected tobe suboptimal, or recovered only after valuable habitatdestruction, for example, rainforests. Can plants for bio-fuel/biomass be grown efciently enough under theseconditions? Is it environmentally desirable to do so? It is,therefore, timely to ask whether articial photosynthesismight be an important alternative route to the efcientproduction of solar fuels. In this and the following sec-tions, an attempt is made to outline questions that must

be answered, and the choices to be made, before startingto design systems capable of performing articial photo-synthesis. Is it possible to think about using the naturalpigment protein complexes/enzymes in the constructionof such articial systems? In our view the natural proteins

are not robust enough for use in systems that will beneeded to work reliably for years at a time without repairand replacement. The natural process of photosynthesisis successful because plants have developed a battery oprotective and replacement strategies so that damage iskept to a minimum and, where it cannot be avoided,nonfunctional components are continually replaced.Under strong illumination Photosystem II, for example,is replaced every 30 min or so[14] . However, along theroad to achieving articial photosynthesis the use of natu-ral proteins, as functionally competent modules capableof carrying out the various steps in the photosynthetic

process, will undoubtedly be very useful tools with whichto investigate the design principles involved in assemblingsystems capable of making solar fuels. Readers interestedin obtaining more detailed information on articial pho-tosynthesis are directed to a special issue of Accounts ofChemical Research that was devoted to this topic[15] .

The light concentration stepThere are now high-resolution x-ray crystal structuresof many different light-harvesting pigment proteincomplexes[16] . So it is possible to ask whether there areany strongly conserved structural features that couldgive clues on the best way to construct articial lightharvesting arrays.Figure 2 shows the structures of sev-eral different types of antenna complexes. The strik-ing feature of this comparison is that they are all verydifferent. At rst glance there do not appear to be anystrongly conserved features. The relative arrangement ofthe pigments varies and there are no strongly conservedprotein folds. Why is this, especially, as we will see inthe following section, when the opposite is true for reac-tion centers? The answer lies in the physics of energytransfer. When a pigment molecule, such as chlorophyll,is excited by the absorption of a photon a molecularclock starts ticking. It stops when the energy stored inthe excited state is lost by decay back to the ground state.For monomeric chlorophyll in solution this decay takesplace in approximately 1 ns. Productive energy trans-fer must occur faster than this. In most photosyntheticantenna systems the time taken for the excitation energyto move from the antenna chlorophylls to the reactioncenter is at most a few hundred ps[16] . The rates ofenergy transfer depend upon factors such as the distancebetween the pigments, the relative angles between thetransition dipole moments of the donor and acceptormolecules (an orientation factor), the spectral overlapbetween these transition dipoles (an energy gradient

Key term

Solar fuel: Fuels are those made usingthe energy incident on the Earthssurface that originates from the sun.


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factor) and the excited state lifetime of the donor excitedstate[16] . In more general terms, the stronger the cou-pling between the donor and acceptor molecules, thefaster the rate of energy transfer. However, the overallrate of energy transfer can vary a lot and yet this process

can still be efcient, as long as this rate out-competes1 ns. There are, therefore, many different ways to orga-nize light-harvesting pigments while still retaining theproperty of efcient energy transfer. During evolutionthere have clearly been many solutions to the problemof assembling an efcient light harvesting system[16] .

Figure 3 shows some of the types of articial antennasystems that have been synthesized. Most of these thatshow efcient energy transfer to a trap (equivalent to areaction center), have been linked together covalently.Interestingly, biology does not usually attach its light-harvesting pigments to the antenna proteins with cova-

lent bonds. If, as we suggest, the construction of arti-cial antenna complexes is not too difcult, is it possibleto make them more energy efcient? One major prob-lem with the photosynthetic antenna pigments is thateffectively all of their useful photochemistry takes placefrom their rst excited singlet states (i.e., from the redend of the spectrum). Even if a blue (short wavelength,higher energy) photon is absorbed, the excitation energyis only available from the red-most lowest excited singletstate. This is because the rate of internal conversionfrom higher excited states to the lowest excited singletstate is so fast that it out competes any chance of energytransfer or electron transfer from the higher excited sin-glet states. This means that on going from 400700 nm,42% of the energy is lost before chlorophyll undergoesuseful photochemistry. Will it be possible to avoid thisproblem and use pigments that absorb in the blue spec-tral region and do their photochemistry there, or absorbin the green and do their photochemistry there and soon? If this does prove to be possible, then the overallefciency will rise because the 42% of the energy cur-rently just wasted could then be utilized. This is the ideabehind the multijunction, multiphoton solar cells[101] .In this case, theoretical energy conversion efcienciesare close to 50%.

Another important question to be considered is whatis the longest wavelength (the lowest energy) that canbe used? If one of the major aims is to be able to oxidizewater then there must be enough energy in the photonto produce the approximate -1.23 V required to achievethis. There are also thermodynamic considerations thatmust be taken into account, with the result that onlyapproximately 70% of the energy of the photon can bestored in a charge separation event without debilitatinglosses from back reactions. This effectively means thatwavelengths below 700 nm cannot be harnessed to driveoxygen evolution. Coupled to this is the requirement to

produce reducing equivalents that are reducing enoughto be used to synthesize the fuel. In photosynthesis thisrequires the involvement of two separate reaction centers. Will an articial system also need two charge separationsteps? The answer is, again, not yet clear.

Photosynthetic light-harvesting systems consist oflarge supramolecular arrays of antenna complexes. Thesearrays self-assemble and are sometimes highly orderedbut sometimes less so. A challenge for articial antennasystems is to progress from individual functional units tolarge arrays of these units whilst retaining efcient energytransfer to the required traps. As yet, most of the articialantenna mimics have not been organized into the largearrays that will be needed for any serious scalable device.Interesting work is being done in this area using naturalantenna complexes from purple bacteria, tagging themwith cysteine residues and using these to attach to orderedarrays of gold atoms on surfaces[17] . This approach couldalso be applied to articial antenna molecules if they too

CB

D E

A

a c

b

Figure 2. Comparison of the structure of photosynthetic light-harvestingcomplexes. (A) Rhodopseudomonas acidophila 10050 LH2 (PDB: 1KZU[52]) isviewed from the side parallel with the membrane plane, and (B) top-waysfrom the N-terminal side. Cyan: the a -apoprotein; green: the b -apoprotein;red: B850 bacteriochlorophyll (Bchl) as; blue: B800 Bchl as; and orange: thecarotenoid rhodopin-glucoside. (C) The peridinin-chlorophyll-protein from Amphidinium carterae (PDB: 1PPR[53]). Silver: apoprotein; red: chlorophyll(Chl) a; orange: the carotenoid peridinin; cyan: digalactosyl diacyl glycerol.(D) The FennaMatthewOlson protein from Prosthecochloris aestuarii (PDB: 3EOJ[54]). Magenta: Bchl as; yellow, red and green: the apoproteinb -sheet, helices and loop., respectively. (E) Light-harvesting complex (LHC)II from pea plant ( Pisum sativum ) (PDB: 2BHW[55]). The LHCII is viewed in

trimeric complex. Each monomer is colored pink, yellow and dark green. The three transmembrane helices (a, b and c) present in a monomer arelabeled. The Chl a and b molecules are in red and green, respectively.Orange: the carotenoids; blue: lipids.


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are tagged. Furthermore, the assembly of articial sys-tems under nonequilibrium conditions, possibly those ofhigh light ux, may possibly offer an interesting route forthe assembly of more efcient and functional systems.

It is important to ask at this time whether light-har-vesting systems are actually required for efcient photo-synthesis, either natural or articial, or indeed whetherthey could even be detrimental. For many plants, toomuch light rather than too little light seems to be theproblem. At light intensities much below those of fullsunlight, the rate of photosynthesis saturates and theexcess light energy is mainly dissipated by nonphoto-chemical quenching. As a consequence, research is nowbeing conducted to see if photosynthesis can be moreefcient at high light intensities if the size of the antenna

system is reduced. At subsaturating light intensities ofcourse the case for light-harvesting complexes is clear.If the efciency of the conversion of total incident lightenergy into fuel is important, as we have suggestedabove, then light harvesting is also important in orderto be able to absorb a wider range of incident wave-lengths. Interestingly, Grtzel is trying to increase theoverall efciency of his solar cell by including antennapigments in order to try to absorb photons over a largerrange of wavelengths (personal communication). Theissue of light-harvesting capacity is therefore compli-cated and what is an optimal size for each reactioncenter will depend upon many different factors, includ-ing how fast the downstream reactions can cope withthe output of the reaction centers.

Zn

Zn

Zn

h

Zn

R

NH

NH

NH

NH

NH

NHNH NH

NH

NH

HN

NH NH

NH

NH

HNR

R

R

R

R

R

O O

O

O

ORR

R

R

OROR

R

R =

R 1 =

R R

R

R

NN

N

NN

NN

NN

NN

NN

N

RR

R

RH 2

1

1

1

1

1

1

A B

C

Figure 3. Examples of articial antenna complexes. (A) An antenna-mimic molecule based on a small, covalently linked network ofporphyrins. The arrows show the direction of energy transfer, which occurs from the Zn porphyrins to the central free-base porphyrin.(B) Poly(propylene imine) dendrimers modied with p -conjugated oligo( p-phenylene vinylene)s [57] . (C) A more elaborate attempt toproduce an antenna mimic based on the LH2 structure from purple bacteria. In this case, a calix arenoporphyrin, which dimerizes togive the molecular structure depicted in this gure, has been designed to produce a model of the tightly coupled bacteriochlorophyllsseen in LH2. Figures (A) and (B) reproduced with permission from [56] .


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The charge-separation step A comparison of the x-ray crystal structures of the dif-ferent types of reaction centers reveals that they are veryhomologous(Figure 4) . Moreover, the organization of thedifferent redox components in them is, essentially, the

same. This reects the fact that the structural require-ments for efcient unidirectional electron transfer arevery strict. Each reaction center contains a short chainof redox carriers that are arranged such that the edge-to-edge distances between them in the different types ofreaction centers are almost identical. These chains arerequired to ensure a stable charge separation and pre-vent energy-wasting back reactions. In reaction centersfrom the purple bacteriumRhodobacter sphaeroides , forexample, with each forward step along the chain, the backreaction is slowed down by three orders of magnitude[18] .In photosystem II and the purple bacterial reaction cen-

ters the electron transport only goes down one of the twoarms. By contrast, in photosystem I both arms are active.Very recently, it has been suggested that this may reducethe driving force required[19] . If this proves to be truethen modied reaction center mimics with more thanone electron transfer arm should be tested.

There have been many reaction center mimics syn-thesized[20] . A typical example of these is given inFigure 5 . It is possible to make single donor-acceptorsystems that show light-induced charge separation but,in these simple pairs, the back charge recombinationrate is always very high and the charge-separated stateis, therefore, too short to allow it to be used efciently.Inclusion of extra donors and acceptors, as seen in thenatural photosynthetic system, stabilizes the charge sep-aration so that the separated charges can now be usedproductively. This stabilization does, of course, reducethe redox potential available for subsequent chemicalwork. So far, most of these reaction center mimics can

only undergo a single charge separa-tion event. Oxygen evolution fromwater and the reductive chemistryneeded to make a fuel require theaccumulation of multiple charges.

Strategies about how to constructreaction center analogs that havemultiple turnover cycles coupled with the capacity tostore several charges at once are only recently being con-sidered. Photosystem II uses a manganese cluster to storethe four positive charges that result from the four single,one photon-induced turnovers that are needed to oxidizeone molecule of water(Figure 6) [21,22]. Unfortunately, theexact molecular details of thewater splitting reactionremain to be elucidated. This problem is, perhaps, themajor unsolved mystery in photosynthesis.

Devising light-driven charge separation devices

that are able to couple one-electron turnover reac-tions to chemical reactions requiring multiple chargesis a major current barrier in solar fuel-based articialphotosynthesis research. It would be a major break-through if it proves possible to couple these reactionsto photoelectrochemical systems such as solar cells.

Catalysis: water splitting & synthesis of a fuelPhotosynthetic organisms have evolved to split waterto release reducing equivalents. The rst step of thisextremely intricate chain of chemical reactions occurson the donor side of photosystem II. Recent advancesin the structural determination of the active site of thisenzyme have conrmed the presence of a manganese-oxocluster along with some other elements in close proximity[21,22] . The cluster, together with surrounding species, isknown as the oxygen-evolving center (OEC)(Figure 7) .The role of the other elements (Ca 2+ and Cl-) is still muchdebated. However, it has been known for a number of

A

B C

HB

QB Q A

HA

BAP

BBCar

Fe 2+

QA QB

B3

A2

B1A1

B2

A3

FAFB

FX

Car D1Pheo D1

Chiz D1

ChlD1 Chl D2

Pheo D2

Car D2

Chiz D2TyrD

TyrZ

QA QB Cyt b-559

Cyt b-550

Mn4Ca cluster

P D1 P D2

Fe 2+

Figure 4. Comparison of the component co-factors of the electron transport chain with the polypeptide removed in the reactioncenter. From (A) Blastochloris viridis (PDB:2PRC)[58], (B) photosystem I (PS I) from cyanobacterium Synechoccus elongates (PDB:1JB0)[59] and (C) photosystem II (PSII) from Thermosynechococcus elongates (PDB:2AXT)[60].

Key term

Water splitting: The key reactionwhereby photosynthesis is able toextract electrons from water that areultimately used to reduce carbondioxide to carbohydrate.


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years that the OEC is rstly oxidized in a series of one-electron steps. This oxidized complex splits the water intomolecular oxygen, protons and reducing power in theform of electrons. This sequence of events is known asthe Kok cycle(Figure 6) [23] .

The OEC overcomes the two main challenges ofthe water oxidation process. First, it is capable of stor-

ing and utiliz-ing the oxidativepower requiredto overcome thehigh thermody-namic barrierfor water oxida-tion. Second,it provides a

mechanistic pathway for the simultaneous breaking offour hydrogen-oxygen bonds and the formation of thetwo oxygenoxygen bonds(Equation 1) . This is achievedat a rate of six orders of magnitude higher than the bestarticial water oxidation catalyst[24] .Half reaction and potential for water oxidation:

2H2O O2 + 4H++ 4e-E = 1.229 - 0.059 pH (25C)

Equation 1

If hydrogen is the desired fuel, then it is reasonableto ask whether systems just based on the electrolysis ofwater could be used to split water? Conventional solarcells could then be employed to drive this process.Unfortunately, there are, at present, signicant prob-lems that make this approach nonoptimal. In theory, the

h h h h S

0S

1S

2S

3S

4

2H2OO

2 + 4H +

Figure 6. The Kok cycle [23] .

H 39 C 16C 8 H 17

C 8 H 17

C 16 H 39

C 16 H 39

OO

O

O

O

O

H39

C16

H 17 C 8

H 17 C 8

N N N

N N

N NN

A

B

Figure 5. Photochemical electron donor-acceptor triads having an aminopyrene primary donor (APy) and p-diaminobenzenesecondary donor (DAB) attached to both imide nitrogen atoms of a perylene-3,4:9,10- bis (dicarboximide) (PDI) electronacceptor were prepared to give (A) a DAB-APy-PDI-APy-DAB monomer. (B) Side-viewed structure of its self-assembled hexamer inmethylcyclohexane as determined by small angle x-ray scattering/wide angle x-ray scattering.Reproduced with permission from [61] .


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minimum electric potential required to split water intooxygen and hydrogen is -1.23 V, under standard condi-tions of 25C and pH 7.0. In practice, there is a largeoverpotential, usually between 0.5 and 0.7 V. This over-potential can be reduced with the use of noble metal

catalysts. Current systems for using photovoltaic solarcells to split water, and so produce hydrogen, are bothinefcient and expensive, especially when comparedwith producing hydrogen by steam reforming of natu-ral gas. There is a great deal of research going on to tryto nd better catalysts for water splitting[2427] . If thisprocess is ever going to be scalable at the level requiredto make a major contribution to the worlds energyneeds, then these catalysts will have to involve the useof non-noble metals. There is, for example, not enoughplatinum in the world to allow it to be used in any reallylarge-scale process for water splitting. Photosynthesis

has overcome this problem by using abundant cheapmetals as catalysts for water splitting. Any sensible sys-tem for articial photosynthesis must do likewise andemploy common elements, such as manganese or iron.Readers interested in getting more information on thispoint should visit[106] , where the Center for ChemicalInnovation-SOLAR project, directed by Harry Gray, isdescribed. This is one of their major aims.

As water oxidation involves a multielectron transferprocess, the water splitting catalysts invariably includea transition metal in their structures. They can be dif-ferentiated in terms of their mode of action (homo-geneous vs heterogeneous) and also according to thekind of ligands coordinating the redox-active transitionmetal (organic vs inorganic) or their bonding pattern(framework vs molecular).

The design of homogeneous catalysts is more ame-nable to approaches that provide insights into the reac-tion mechanism. These types of catalysts, therefore, areeasier to develop by building on information gainedfrom spectroscopic, kinetic and theoretical analysis ofthe natural system. On the other hand, heterogeneouscatalysts are generally more robust towards oxidativedegradation and easier and more economical to fabri-cate[28] . Moreover, heterogeneous catalysts can be inte-grated more easily into devices that are able to couplethe water oxidation process to proton reduction (andso achieve the splitting of water into molecular oxygenand hydrogen). See Brimblecombeet al. for an exampleof this[29] .

One special class of materials that have a great deal ofpotential for use as both homogenous and heterogenouscatalysts for water splitting are based upon a class of mate-rials calledpolyoxometalates (POMs).Table 1 shows thestructures and main features of some molecular catalystsfor water oxidation from the more well-known organo-metallic systems to POMs[24] . POM-based catalysts,

have recentlyburst onto thescene and mades i g n i f i c a n timprovements

in terms of rateand turnover[28,3032] . POMsare metaloxy-gen anion clus-ters that havegiven rise to agreat deal ofexcitement dueto their oxidative stability, solubility properties andelectronic tuneability. All these features suggest thatthis new class of water oxidation catalysts could revolu-

tionize the eld. In this respect, many groups, includingour own, are currently investigating these systems, andattempting to design new catalytically active clusters.To do this effectively requires a degree of structuralcontrol. Their structures were traditionally described asan assembly of (MOx ) units where M = Mo, W, V andNb, and x = 47. Recent discoveries have expanded thePOM family to clusters including noble metals such as Au and Pd[33,34] . Research in the eld is growing almostexponentially, owing to the wide range of physical prop-erties, topologies and sizes of these types of clusters. Anumber of reviews have been published in the last fewyears that give an excellent account of their propertiesand applications[3537] .

Polyoxometalates can be separated into heteropoly-anions and isopolyanions. Heteropolyanions pos-ses a central anion, such as SO42- or PO43-, which isthought to template the assembly of the POM in solu-tion. Isopolyanions lack this core anion/atom. Thetwo most important structural types within the het-eropolyanions are the stable Keggin [XM12O40]n- and WellsDawson [X 2M18O62]n- anions (where M = Wor Mo and x is a tetrahedral template)[36] . Lacunaryheteropolyanions derive from these through the lossof one or more of the metal atoms along with theunshared O2- ligands, usually upon treatment withbase[38] . They are ideal inorganic ligands as they read-ily coordinate other metal centers in order to ll thesevacancies and, hence, regain the stability of the parentstructure. When the coordinated species is a transitionmetal they are know as transition metal-substitutedpolyoxometalates (TMSPs).

One of the most successful lacu-nary POMs, in terms of the numberof new structures obtained by usingit as a synthetic precursor, is the poly-oxoanion [SiW 10O36]8- [(SiW 10)].

Glu 189

Glu 354Glu 333His 332

Mn

Ca

O

O

O

O

MnMnMn

Ala 344Asp 170

Asp 342

Figure 7. Oxygen-evolving center in photosystem II.Reproduced with permission from [62] .

Key term

Polyoxometalates: Clusters of metaloxygen units usually containinghigh-oxidation s tate metals Mo, W, or V


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The key to this success is the fact that (SiW 10) is meta-stable in solution[39] . This results in a range of otherlacunary species related to (SiW 10) by isomerizationand/or gain or loss of tungsten-oxo units. Some of thesemolecules can also coordinate other transition metals insolution giving rise to a fantastic structural variety. Thesynthetic procedures employed to produce TMSPs arerather diverse. In the case of one-pot reactions in aqueoussolution, control of certain key variables determines thestructure of the product.

Using this approach we have been able to encap-sulate Mn-cubanes of similar architectures foundin photosystem II, into POM oxide shells. Forexample, a POM ligand system derived from thetri-vacant lacunary (B-a -X IV W VI9O34)10- poly-anion. The resulting clusters contain a central,mixed-valence (Mn6) = [MnII I4MnII2O4(H2O)4]8+ cluster core that is anchored between two rigidlacunary [XW 9O34]10- POM clusters[40] . These spe-cies were isolated as Na 4K(C4H10NO)7([GeW 9O34]2

Table 1. Selected examples of molecular catalysts for water oxidation.

Catalyst (homogeneous) Initial turnoverfrequency (x10 -3 s -1)

Turnovernumber(mol O 2/mol cat)

Sacricial oxidant Ref.

Meyer, 1982

[(bpy)2(H2O)RuORu(H2O)(bpy)2]4+

10.0 13.2 Ce(IV) [63]

Llobet, 2004

[Ru2(-OAc)(bpp)(trpy) 2]2+

25.9 18 Ce(IV) [64]

Thummel, 2005

trans,trans -[Ru2(-Cl)(-binapypyr)-(4-Me-py)4]3+

0.1 3200 Ce(IV) [65,66]

Bernhard, 2007

[Ir(ppy)2(H2O)2]+

7.54 2500 Ce(IV) [66]


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[MnII I4MnII2O4(H2O)4]) see Figure 8 . Their abil-ity to catalyze the oxidation of water is currentlybeing assessed.

Nocera has recently reported on thein situ formationof an oxygen-evolving catalyst upon anodic polarizationof an inert electrode in phosphate-buffered water con-taining cobalt (II) ions[41] . A dark coating forms on thesurface of an indium-tin oxide electrode after electrolysisat 1.29 V in a neutral KPi electrolyte (potassium phos-phate pH 7) containing 0.5 mM Co2+. The composition

of this electrodeposited material was analyzed using dif-ferent experimental techniques. First, energy-dispersivex-ray analysis spectra were obtained and identied Co,P, K and O as the principal elemental components ofthe material. Electrolysis using large indium-tin oxideelectrodes allowed microanalytical elemental analysis ofthe material and results indicated roughly a 2:1:1 ratiofor Co:P:K. Finally, x-ray photoelectron spectroscopywas used to analyze the surface of the electrodepositedmaterial. The analytical results combined indicate that

Table 1. Selected examples of molecular catalysts for water oxidation (cont.).

Catalyst (homogeneous) Initial turnoverfrequency (x 10 -3 s-1)

Turnovernumber(mol O 2/mol cat)

Sacricial oxidant Ref.

Crabtree, 2009

Cp*Xlr

N

1a, X = Cl

900 >1500 Ce(IV) [67]

Hill/Bonchio, 2008

(Ru4)(SiW10)2

37.0 385 [Ru(bpy) 3]3+ [31,32]

Hill, 2010

(Ru4)(PW10)2

130 120 [Ru(bpy) 3]3+ [68]

Hill, 2010

(Co4)(PW9)2

5000 1000 [Ru(bpy) 3]3+ [28]


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Executive summary

The case is made for clean renewable systems to make fuels rather than just electricity. Photosynthesis is the one major chemical/biochemical process on earth that does make fuels renewably. Solar energy is an abundant source of energy but it is also a low-density source. This makes it important to consider how efficiently solar

energy can be converted into a fuel. The lower the efficiency the larger the sur face area required for light harvesting. There is often confusion with the denition of efficiency. All the efficiencies quoted in this review have been calculated on the basis of

comparing the total energy input with the total energy output. The maximum efficiency of the conversion of solar energy into biomass by plants is 4.6% for C3 photosynthesis and 6% for C4 photosynthesis. Photosynthesis can be broken down into four partial reactions.

Strategies for building systems based on articial photosynthesis for producing solar fuels can be constructed by analyzing each of thesefour partial reactions.Recent progress in determining structural function of the photosynthetic pigment protein complexes responsible for carrying out lightharvesting and charge separation have informed the design of articial mimics of both of these steps in the photosynthetic process.

The major hurdles to be overcome in achieving articial photosynthesis are producing catalysts capable of splitting water and reductivesynthesis of fuels.

Current molecular catalysts for water splitting are described, and prospects for the synthesis of better ones are discussed based uponpolyoxometalates.

Enzymes such as hydrogenase and formate dihydrogenase that could be used to make fuels are discussed. The major problem of how to reduce atmospheric carbon dioxide to a hydrocarbon fuel is highlighted.

of solar fuel but because it highlights the importance ofcompartmentalization. Photosynthesis relies upon thisand it is highly probable that compartmentalization willalso be required to be part of the design of any practicalarticial system capable of producing solar fuels.

Future perspective Articial photosynthesis holds out the promise of beingable to provide an efcient way of producing solar fuels. As outlined above, using the conceptual framework ofbreaking down photosynthesis into its four general stepsprovides a focused way to attack the problem of mak-ing robust systems for replicating each of these stages.Currently, the most challenging bottlenecks to theachievement of even microscale systems for solar fuel pro-duction based on articial photosynthesis are the catalyticsteps needed for water oxidation and fuel production.

We are not daunted by these problems. Rather, we areencouraged since more and more talented researchers arenow rising to this challenge.

We expect that during the next 10 years, the crystal-lography of photosystem II will be greatly improved. As a result of this the structure of the OEC will bedetermined to high resolution in each of the differ-ent S states. This will reveal the secrets of the precisemechanism of the water splitting reaction. The role ofthe protein will then be precisely determined. This willprovide the blueprint for synthetic chemists to design anew generation of catalysts that will place the mimic ofthe OEC into a smart matrix that will truly replicatethe catalytic power of the natural system. Biology hasevolved by changing the matrix (the protein) and thisis why enzymes are such remarkable catalysts.

Biology uses self-assembly and self-repair to producelong-term stability in processes such as photosynthesis.

Articial photosynthesis will also probably need to usethese techniques if it is to become scalable. This idea hasbeen considered before but has not yet become a seriousresearch focus. We expect this will change rapidly in thenext few years. Processes such as water splitting involve

highly dangerous oxidizing species. Self-repair will there-fore be important to build into any device that splits waterand is required to have a long lifetime (namely, years).

Many of the enzymes that can be harnessed to producefuels, such as hydrogenase or nitrogenise, are currentlyvery oxygen sensitive. We expect the molecular details ofthis oxygen sensitivity will be elucidated and modiedenzymes capable of producing hydrogen in the presenceof oxygen will be produced. Most probably thermophilicvarieties of these enzymes will be used as they will haveenhanced stability.

We expect that during the next 10 years, small dem-

onstration systems will be constructed based on articialphotosynthesis that can make solar fuels. Research in thisarea is at a fascinating stage. We know what we want toachieve. We know the end point we want to reach. Whatwe do not yet know, is how to get there. However, sincebiology obeys the same rules of physics and chemistry, asall other processes on earth, if we have sufcient insightinto the biological process then it must be possible to rep-licate it. This rationale provides the hope not only for thisarea of research, but for our future on this planet. Oneof the grand challenges mankind faces is to devise waysfor the sustainable production of carbon-neutral fuels.The benets for addressing climate change is clear, thisapproach could give rise to a technology that would takethe fossil out of the fuel, allowing real-time recyclingof carbon dioxide, negating the need to access harder-to-extract and dirtier forms of fossil fuel for when oil andgas run out.


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32 Geletii YV, Botar B, Koegerler Pet al. Anall-inorganic, stable, and highly activetetraruthenium homogeneous catalyst forwater oxidation. Angew. Chem. Int. Ed. 47,38963899 (2008).

33 Izarova NV, Vankova N, Heine Tet al. Polyoxometalates made of gold:the polyoxoaurate [(Au4 As4O20)-As-III-O-V]8-. Angew. Chem. Int. Ed. 49, 18861889(2010).

34 Chubarova EV, Dickman MH, Keita Bet al. Self-assembly of a heteropolyoxopalladatenanocube: [(Pd13 As8O34)-As-II-O-V(OH)6]8-. Angew. Chem. Int. Ed. 47, 95429546 (2008).

35 Hill CL. Introduction: polyoxometalatesmulticomponent molecular vehicles to probefundamental issues and practical problems.Chem. Rev. 98, 12 (1998).

36 Long D-L, Tsunashima R, Cronin L.

Polyoxometalates: building blocks forfunctional nanoscale systems. Angew. Chem.Int. Ed. 49, 17361758 (2010).

37 Long D-L, Burkholder E, Cronin L.Polyoxometalate clusters, nanostructures andmaterials: from self assembly to designermaterials and devices.Chem. Soc. Rev. 36,105121 (2007).

38 Baker LCW, Glick DC. Present general statusof understanding of heteropoly electrolytesand a tracing of some major highlights in thehistory of their elucidation.Chem. Rev. 98,349 (1998).

39 Canny J, Teze A, Thouvenot Ret al. Disubstituted tungstosilicates. 1. Synthesis,stability, and structure of the lacunaryprecursor polyanionG-Siw10o368-.Inorg.Chem. 25, 21142119 (1986).

40 Ritchie C, Streb C, Thiel Jet al. Reversibleredox reactions in an extendedpolyoxometalate framework solid. Angew. Chem. Int. Ed. 47, 68816884(2008).

41 Kanan MW, Nocera DG.In situ formation ofan oxygen-evolving catalyst in neutral watercontaining phosphate and Co2+. Science 321,10721075 (2008).

n Describes the formation and performance ofa novel oxygen-evolving catalyst. Itrepresents a major step forward in this area.

42 Vignais PM, Colbeau A, Willison JCet al. Hydrogenase, nitrogenase, and hydrogenmetabolism in the photosynthetic bacteria. Adv. Microbiol. Physiol. 26, 155234 (1985).

43 Sasikala K, Ramana CV, Raghuveer Rao Pet al. Anoxygenic phototrophic bacteria:physiology and advances in hydrogenproduction technology. Adv. Appl. Microbiol . 211295 (1993).

44 Shima S, Pilak O, Vogt Set al. The crystalstructure of [Fe]-hydrogenase reveals thegeometry of the active site.Science 321,572575 (2008).

45 Garcin E, Vernede X, Hatchikian ECet al. The crystal structure of a reduced [NiFeSe]hydrogenase provides an image of theactivated catalytic center.Structure 7,557566 (1999).

46 Fontecilla-Camps JC, Volbeda A, Cavazza Cet al. Structure/function relationships of[NiFe]- and [FeFe]-hydrogenases.Chem. Rev. 107, 42734303 (2007).

47 Masepohl B, Kranz RG. Regulation ofNitrogen xation. In:The PurplePhototrophic Bacteria . Hunter CN, Daldal F,Thurnauer MCet al. (Eds). 759775Springer, Dordrecht, The Netherlands(2009).

48 Parkinson BA, Weaver PF.Photoelectrochemical pumping ofenzymatic CO2 reduction.Nature 309,148149 (1984).

49 Obert R, Dave BC. Enzymaticconversion of carbon dioxide to methanol:enhanced methanol production in silicasol-gel matrices. J. Am. Chem. Soc. 121,1219212193 (1999).

50 Reda T, Plugge CM, Abram NJet al. Reversible interconversion of carbon dioxideand formate by an electroactive enzyme.Proc.Natl Acad. Sci. USA 105, 1065410658 (2008).

51 Wendell D, Todd J, Montemagno C. Articial photosynthesis in ranaspumin-2based foam.Nano Lett. 10(9), 32313236 (2010).

52 Prince SM, Papiz MZ, Freer AAet al. Apoprotein structure in the LH2 complexfromRhodopseudomonas acidophila strain10050: modular assembly and proteinpigment interactions. J. Mol. Biol . 268,412423 (1997).

53 Hofmann E, Wrench PM, Sharples FPet al. Structural basis of light harvesting bycarotenoids: peridinin-chlorophyll-proteinfrom Amphidinium carterae . Science 272,17881791 (1996).

54 Tronrud DE, Wen JZ, Gay Let al. Thestructural basis for the difference inabsorbance spectra for the FMO antennaprotein from various green sulfur bacteria.Photosyn. Res. 100, 7987 (2009).

55 Standfuss R, van Scheltinga ACT,Lamborghini Met al. Mechanisms ofphotoprotection and nonphotochemicalquenching in pea light-harvesting complexat 2.5A resolution.EMBO J. 24, 919928(2005).

56 Cogdell RJ, Lindsay JG. Can photosynthesisprovide a biological blueprint for the desigof novel solar cells?Trends Biotechnol. 16,521527 (1998).

57 Schenning APHJ, Peeters E,Meijer EW. Energy transfer in supramolecuassemblies of oligo(p-phenylene vinylene)sterminated poly(propylene imine)dendrimers. J. Am. Chem. Soc. 122,44894495 (2000).

58 Lancaster CRD, Michel H. Thecoupling of light-induced electron transferand proton uptake as derived from crystalstructures of reaction centers fromRhodopseudomonas viridis modied at thebinding site of the secondary quinone, Q(B)Structure 5, 13391359 (1997).

59 Jordan P, Fromme P, Witt HTet al. Three-dimensional structure of

cyanobacterial photosystem I at 2.5 resolution.Nature 411, 909917 (2001).60 Loll B, Kern J, Saenger Wet al. Towards

complete cofactor arrangement in the 3.0 resolution structure of photosystem II.Nature 438, 10401044 (2005).

61 Bullock JE, Carmieli R, Mickley SMet al. Photoinitiated charge transport throughpi-stacked electron conduits insupramolecular ordered assemblies ofdonor-acceptor triads. J. Am. Chem. Soc. 131,1191911929 (2009).

62 Siegbahn PEM. An energetic comparison ofdifferent models for the oxygen evolvingcomplex of photosystem II. J. Am. Chem. Soc. 131, 1823818239 (2009).

63 Gersten SW, Samuels GJ, MeyerTJ. Catalytic-oxidation of water by anoxo-bridged ruthenium dimer. J. Am. Chem.Soc. 104, 40294030 (1982).

64 Sens C, Romero I, Rodriguez Met al. A new Ru complex capable ofcatalytically oxidizing water to moleculardioxygen. J. Am. Chem. Soc. 126, 77987799(2004).

65 Zong R, Thummel RP. A newfamily of Ru complexes for wateroxidation. J. Am. Chem. Soc. 127, 1280212803 (2005).

66 McDaniel ND, Coughlin FJ, Tinker LLet al. Cyclometalated iridium(III) aquocomplexes: efcient and tunable catalystsfor the homogeneous oxidation of water. J. Am. Chem. Soc. 130, 210217 (2007).

67 Hull JF, Balcells D, Blakemore JDet al. Highly active and robust Cp*iridium complexes for catalytic wateroxidation. J. Am. Chem. Soc. 131, 87308731(2009).


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68 Besson C, Huang Z, Geletii YVet al. Cs9[([g]-PW 10O36)2Ru4O5(OH)(H2O)4], a newall-inorganic, soluble catalyst for the efcientvisible-light-driven oxidation of water.Chem.Commun. 46, 27842786 (2010).

Websites101 Basic research needs for solar energy utilisation

report on the Basic Energy Sciences Workshop on Solar Energy Utilisation (2005).www.sc.doe.gov/bes/reports/les/SEU_rpt.pdf

n Shows the major Department of Energyreport on possible ways to harness solarenergy. It provides a comprehensive state ofthe art picture of research in this area.

102 California Institute of Technology, LEWISresearch group. Global energy perspective.http://nsl.caltech.edu/energy

103 Energy Biosciences Institute.www.energybiosciencesinstitute.org

104 US Department of Energy Ofce of Science.Genomic science program.http://genomicscience.energy.gov/centers/index.shtml

105 European Science Foundation (EFS).Harnessing solar energy for the production ofclean fuel.www.esf.org/publications/science-policy-briengs.html

n Shows the ESF report on solar fuels, withparticular emphasis on the role ofphotosynthesis. The possible uses of bothnatural photosynthetic systems and articialbio-inspired ones are discussed.

106 Center for Chemical Innovation.www.ccisolar.caltech.edu

107 Uppsala University, Department ofPhotochemistry and Molecular Science.www.fotomol.uu.se/Forskning/Biomimetics/solarh

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