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REVIEW

Artificial photosynthesis solar fuels: current status and future prospects

Biofuels (2010) 1(6), 861876

Richard J Cogdell1*, Tatas HP Brotosudarmo1, Alastair T Gardiner1, Pedro M Sanchez2 &LeroyCronin2*

This review considers the case for using artificial photosynthesis to make solar fuels. The conceptual framework on which this idea is based is described. Photosynthesis is broken down into four partial reactions. Each one is described and progress in mimicking each of these is discussed. Finally, the current major barriers to achieving working systems based on artificial photosynthesis capable of making solar fuels are highlighted.

There is currently a great deal of research interest aimed at developing clean, sustainable sources of energy. Unfortunately, most of this research is only focused on producing electricity. A much more challenging target is to try and develop novel ways of producing fuels [101] . Currently, in the developed world, approximately 70% of our energy comes from the combustion of fuel [1] . Clean electricity generation is a worthwhile aim in itself but is not the complete answer. There are many things we currently do that require a dense, portable fuel, for example, ying long distances and sailing large ships that cannot be accomplished with electricity alone [2,3] . So, how can we make fuel? There is one sustainable process on Earth that does make fuel. This process is photosynthesis and uses solar energy to power fuel production (in this case carbohydrates). This is the reason why there is the drive to use plants to produce so-called biofuels. Most of the current systems designed to do this either take photosynthate in the form of fermentable sugars and convert these into ethanol or produce biodiesel from plant-derived oils. On the face of it this would seem to be a good idea. However, two fundamental questions must be addressed. First, does the fuel give back more energy than originally expended to make it and, secondly, how efciently is solar energy converted into
1 2

fuel [101] ? Until the mid-1990s it cost more energy to make bioethanol than was recovered in the product. Since then, both agricultural and fermentation practices have improved so that the net energy gain is now approximately 36% when US corn is used and rather higher with Brazilian sugarcane [4] . The second question is also a key one because solar energy, although an abundant source of energy (4.31020J reaches the surface of the Earth every hour, which is currently more than mankind uses every year), is rather dilute. In other words, although the total amount of solar energy reaching the Earth is large, the energy incident on any given square meter of the planets surface over time is diffuse and low. In the USA, the average insolation is approximately 200W/m 2. This means that any scalable system that uses solar energy in signicant quantities must harvest that energy over quite large areas of land. This requirement for land must not be forgotten since, as is discussed below, it raises many social and political issues. Artificial photosynthesis could, in principle, be capable of using solar energy to make clean fuels at attractively high efciencies. The main part of this article, which is aimed at a scientically literate general audience, considers the prospects for this and details the major hurdles that need to be overcome if this goal is to become a reality.

Division of Biochemistry & Cell Biology, FBLS, University of Glasgow, GBRC Building, 126 University Place, Glasgow, G12 8TA, UK School of Chemistry, WestCHEM, University of Glasgow, Glasgow, G12 8QQ, UK Author for correspondence: Tel.: +44 141 330 4232; Fax: +44 141 330 4620; E-mail: richard.cogdell@glasgow.ac.uk * Both authors contributed equally to this work.

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The importance of efficiency At this point there will be a small digression about efciency. Different groups of scientists quote different types of efciency and this can lead to a degree of confusion Bioethanol: Ethanol that is produced by [101] . Often researchers who study the fermentation of plant sugars. The the early reactions of photosynthesis impure ethanol is then distilled to produce a product that can be added quote quantum efciency (QE). QE to supplement petroleum products for is dened as the percentage of the use in transportation. number of absorbed photons that Artificial photosynthesis: The assembly produce the reaction. In the case of of chemical systems, the construction the light reactions of photosynthesis, of which is inspired by biology, that are the QE of charge separation in the capable of mimicking the main stages of photosynthesis. reaction center is very nearly 100%. Biologists who study whole-plant C3 plants: Plants such as spinach that initially fix carbon dioxide into a photosynthesis usually use a mea3-carbon sugar, 3-phosphoglyceric acid. sure of efciency that is dened as C4 plants: Plants such as sugarcane that the energy of the biomass produced initially fix carbon dioxide into 4-carbon divided by the total energy of the acids, such as oxaloacetic acid. photosynthetically active radiation (PAR, this means only the fraction of the incident solar radiation that plants can absorb) absorbed. Physicists who study solar cells dene efciency as the energy output of the cell divided by the total energy available from the incident solar radiation on the surface of the cell. The efciencies quoted here have been calculated on the same basis as that used by the physicists. Efciencies with solar cells of between 10 and 20% can be readily obtained [101] . The magnitude of these efciencies represents the extent of the challenge that articial photosynthesis must meet. Currently, mankind consumes 4.11020J per year. Nathan Lewis has calculated how much of the surface of the USA would need to be covered with solar energy collectors 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 energy into fuel, then the larger the surface area required. Any proposed solar energy conversion system must be socially acceptable. If the land area requirements are too large then this becomes a real problem. Current crops used for biofuels are already competing for land with those grown for food or promoting habitat destruction, so the advisability of doing this has been seriously questioned. This controversy will get even worse should this process be scaled up to the level required for the current generation of biofuels to be major sources of energy. When grown under optimum conditions, the maximum efciency of conversion of solar energy into total biomass has been estimated to be 4.6% in C3 plants and a little higher in C4 plants at 6% [5] . However, only a fraction of this biomass can be currently converted into, for example, bioethanol. This results in an even
Key terms Photosynthesis: The biological process found in plants, algae and some bacteria that uses solar energy to convert carbon dioxide into carbohydrate.

lower energy conversion efciency, so, correspondingly, a greater land area is needed. Current estimates of the average efciency of conversion of solar energy into fermentable biomass are approximately 0.3%. To use plants at this level of efciency to produce all our energy needs would require approximately 31% of the total land area of our planet [102] . The cost of producing fuels such as bioethanol must also be considered. Box1 shows an interesting breakdown of the costs of bioethanol relative to that of gasoline based on data from March 2006. The two points to note are the importance of the subsidy given and the fact that bioethanol production becomes increasingly economically feasible as petrol (gasoline) prices rise. The largest factor determining whether or not bioethanol production makes economic sense is, therefore, the cost of a barrel of oil. This is currently a highly mobile target. Even if so-called rstgeneration bioethanol becomes economic it is an altogether different question to ask whether its production is a good idea or not? However, if more of a plants biomass could be converted to ethanol, then both the efciency of its production would rise and its cost would go down. This explains the drive to make systems that can transform both cellulose and lignin into fermentable substrates. This target is the main aim of the large solar energy research center based at the University of California at Berkeley (CA, USA) and the University of Illinois at Champaign-Urbana (The Energy Bioscience Institute[103] ; IL, USA) and the Department of Energy Centers 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 photosynthesis more efciently [5] ? In order to try and answer this question we need to consider what happens in the photosyntheticprocess. The essence of photosynthesis It is possible to break down photosynthesis into four sequential, partial reactions Figure1 [105] . The rst reaction is light harvesting or light concentration. The second uses this concentrated light to separate charge across a membrane (in photosynthesis this is the function of the reaction centers). The third reaction involves using the accumulated positive charges to oxidize water and the fourth uses the resultant negative charges for reductive chemistry to produce the fuel. Production of the fuel requires a supply of sufciently reducing electrons and water is the most accessible and abundant source for these. The model in Figure1 is of course a simplication since in the natural process reduction of carbon dioxide to carbohydrate not only involves the participation of a second photosystem but also requires ATP. However, it does provide a useful conceptual framework. Clearly, if it

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is possible to intervene in the photo- Box1. Price of corn-based ethanol versus price of gasoline. synthetic process early enough then, Cost of ethanol in 10 midwestern states on March 22, 2006 (US$/gal) 2.342.50 theoretically, the energy conversion Subsidy (American Jobs Creation Act of 2004, PL. 108 357) (US$/gal) 0.51 efciency will be higher. The higher Net cost of ethanol (US$/gal) 1.831.99 the efciency, the smaller the quanEnergy Content (BTU/gal): Gasoline 125,000 tity of land required, and the more Ethanol 76,000 potentially acceptable the s olution Gallons of ethanol per gallon gasoline equivalent 1.6 becomes. Price of ethanol per gallon gasoline equivalent (US$/gal) 2.923.18 Intervening earlier in the light Retail price of regular grade gasoline in Midwest, March 20, 2006 (US$/gal) 2.50 reactions and substituting alternaData from [4]. tives for the dark reactions is the idea behind the concept of articial In both cases the x-ray crystal structures of the enzymes photosynthesis. The term articial photosynthesis can be involved in these processes are known, but also, in both confusing since it has been used in many different ways. cases, the proteins actively participate in the catalytic Often it is used when an attempt is made to mimic any mechanisms involved. As a result, the structure of the single stage of the four shown in Figure1. Here, we have active sites visualized in the protein structures only protried to use this term to refer to mimicking all four stages. vides a single static view. The precise details of what goes Is it possible to use this simplied model of photosynthesis on in the reactions are, therefore, not clear and mimto build robust chemical systems that can mimic natural ics, which are usually rigid, fail. In the case of photo photosynthetic reactions and so use solar energy more ef- synthetic reduction of carbon dioxide to carbohydrate ciently to make a suitable fuel? In recent years a great deal there is also a major problem with the main enzyme of progress has been made in understanding the struc- RUBISCO. This enzyme not only has a rather low afnture and function of the various pigment protein com- ity for carbon dioxide but also has a plexes that catalyze the early reactions of photosynthesis, reaction with oxygen that results in Key term namely the antenna complexes and the reaction centers. the loss of one of the previously xed RUBISCO: Ribulose 15 bis-phosphate Readers interested in this work should consult these two carbon atoms. A great deal of work carboxylase/oxygenase. This is the excellent books [6,7] . In both antenna complexes and reac- trying to improve RUBISCO has primary enzyme that fixes carbon dioxide forming carbohydrates. tion centers the processes of energy transfer and electron been carried out without signicant transfer are essentially temperature independent. In other words, there is no molecular motion involved and Electron transfer Electron transfer the proteins simply act as a scaffold to set the optimum preconditions H+ + CO2 for the energy and electron transfer reactions. The proteins do not play an Antenna active role in these reactions over the Reaction center Harvesting light Catalytic timescale during which they occur. Electron gradient site 2 This means that the x-ray crystal 4 1 2 Hydrogen structures of these pigment protein + Energy complexes can be used as excellent methanol transfer models on which to base the design Catalytic of articial mimics. Indeed, there are site 1 now many examples of such synthetic molecules that can be successfully 3 assembled into systems capable of absorbing solar energy and using it to drive efcient charge separation [812] . The real barriers to producing O2 + A + H+ H2O + HA articial systems capable of mimicking the overall reactions of phoFigure 1. Blueprint for the coupling of an antenna system with a reaction center that is tosynthesis are those associated with coupled with catalytic site 1 and catalytic site 2. Catalytic site 1 oxidizes water whereas being able to replicate the slower catalytic site 2 fixes carbon dioxide. The key issue is to develop modular and configurable routes reactions of water oxidation and to join the various components together. the reductive synthesis of the fuel.

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Key term

Solar fuel: Fuels are those made using the energy incident on the Earths surface that originates from the sun.

progress [13] . Producing new catalysts capable of xing carbon dioxide into a suitable fuel that are able to work at the low concentrations of carbon dioxide present in the atmosphere is a very severe challenge indeed.

Choosing the appropriate fuel Before discussing in more detail proposed strategies for building systems capable of using solar energy to make fuel (solar fuel) , it is important to consider what fuel to try and make. This is important because it will inuence subsequent research strategies and because in different situations different choices may be appropriate. In some cases the answer could be hydrogen but in others a more dense, portable liquid hydrocarbon might be preferable. Hydrogen could be a good fuel for heating and powering automobiles, but not for airplanes. Flying will require the denser liquid hydrocarbons. Choosing to make a fuel that is miscible with water introduces other problems. Methanol and ethanol might be rather easy to make, however, a lot of energy is then needed to distil away these fuels from water to obtain them in sufcient concentration/purity that they are combustible. Self-evidently, these cannot not be fuels of choice if too great an energy input is required simply to get them into a useable form. In the current rush to produce biofuels not enough thought has been given to what is the best type of fuel to aim for. This is a very serious issue indeed. If biofuels are tarred with a bad name in a similar way to genetically modied organisms, then there is a danger that, even after sensible sustainable systems for making solar fuels have been developed, an alienated public opinion will have too much opposition for them to be accepted. Now is the time to engage with the public on these issues so that the ground is well prepared when possible solutions are found. Artificial photosynthesis Although it is sensible to attempt to develop plants that can convert solar energy into biomass/fuels with increasing efciency, there are large barriers that must be overcome in order to achieve this. For example, plants grown for energy would need to be located on land either classed as marginal, where plant growth might be expected to be suboptimal, or recovered only after valuable habitat destruction, for example, rainforests. Can plants for biofuel/biomass be grown efciently enough under these conditions? Is it environmentally desirable to do so? It is, therefore, timely to ask whether articial photosynthesis might be an important alternative route to the efcient production of solar fuels. In this and the following sections, an attempt is made to outline questions that must

be answered, and the choices to be made, before starting to design systems capable of performing articial photosynthesis. Is it possible to think about using the natural pigment protein complexes/enzymes in the construction of such articial systems? In our view the natural proteins are not robust enough for use in systems that will be needed to work reliably for years at a time without repair and replacement. The natural process of photosynthesis is successful because plants have developed a battery of protective and replacement strategies so that damage is kept 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 the road to achieving articial photosynthesis the use of natural proteins, as functionally competent modules capable of carrying out the various steps in the photosynthetic process, will undoubtedly be very useful tools with which to investigate the design principles involved in assembling systems capable of making solar fuels. Readers interested in obtaining more detailed information on articial photosynthesis are directed to a special issue of Accounts of Chemical Research that was devoted to this topic [15] .
The light concentration step

There are now high-resolution x-ray crystal structures of many different light-harvesting pigment protein complexes [16] . So it is possible to ask whether there are any strongly conserved structural features that could give clues on the best way to construct articial light harvesting arrays. Figure2 shows the structures of several different types of antenna complexes. The striking feature of this comparison is that they are all very different. At rst glance there do not appear to be any strongly conserved features. The relative arrangement of the pigments varies and there are no strongly conserved protein folds. Why is this, especially, as we will see in the following section, when the opposite is true for reaction centers? The answer lies in the physics of energy transfer. When a pigment molecule, such as chlorophyll, is excited by the absorption of a photon a molecular clock starts ticking. It stops when the energy stored in the excited state is lost by decay back to the ground state. For monomeric chlorophyll in solution this decay takes place in approximately 1ns. Productive energy transfer must occur faster than this. In most photosynthetic antenna systems the time taken for the excitation energy to move from the antenna chlorophylls to the reaction center is at most a few hundred ps [16] . The rates of energy transfer depend upon factors such as the distance between the pigments, the relative angles between the transition dipole moments of the donor and acceptor molecules (an orientation factor), the spectral overlap between these transition dipoles (an energy gradient

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factor) and the excited state lifetime of the donor excited state [16] . In more general terms, the stronger the coupling between the donor and acceptor molecules, the faster the rate of energy transfer. However, the overall rate of energy transfer can vary a lot and yet this process can still be efcient, as long as this rate out-competes 1ns. There are, therefore, many different ways to organize light-harvesting pigments while still retaining the property of efcient energy transfer. During evolution there have clearly been many solutions to the problem of assembling an efcient light harvesting system [16] . Figure3 shows some of the types of articial antenna systems that have been synthesized. Most of these that show efcient energy transfer to a trap (equivalent to a reaction center), have been linked together covalently. Interestingly, biology does not usually attach its lightharvesting pigments to the antenna proteins with covalent bonds. If, as we suggest, the construction of articial antenna complexes is not too difcult, is it possible to make them more energy efcient? One major problem with the photosynthetic antenna pigments is that effectively all of their useful photochemistry takes place from their rst excited singlet states (i.e., from the red end of the spectrum). Even if a blue (short wavelength, higher energy) photon is absorbed, the excitation energy is only available from the red-most lowest excited singlet state. This is because the rate of internal conversion from higher excited states to the lowest excited singlet state is so fast that it out competes any chance of energy transfer or electron transfer from the higher excited singlet states. This means that on going from 400700nm, 42% of the energy is lost before chlorophyll undergoes useful photochemistry. Will it be possible to avoid this problem and use pigments that absorb in the blue spectral region and do their photochemistry there, or absorb in the green and do their photochemistry there and so on? If this does prove to be possible, then the overall efciency will rise because the 42% of the energy currently just wasted could then be utilized. This is the idea behind the multijunction, multiphoton solar cells [101] . In this case, theoretical energy conversion efciencies are close to 50%. Another important question to be considered is what is the longest wavelength (the lowest energy) that can be used? If one of the major aims is to be able to oxidize water then there must be enough energy in the photon to produce the approximate -1.23V required to achieve this. There are also thermodynamic considerations that must be taken into account, with the result that only approximately 70% of the energy of the photon can be stored in a charge separation event without debilitating losses from back reactions. This effectively means that wavelengths below 700nm cannot be harnessed to drive oxygen evolution. Coupled to this is the requirement to

a b

Figure 2. Comparison of the structure of photosynthetic light-harvesting complexes. (A) Rhodopseudomonas acidophila 10050 LH2 (PDB: 1KZU [52]) is viewed from the side parallel with the membrane plane, and (B) top-ways from the N-terminal side. Cyan: the a-apoprotein; green: the b-apoprotein; red: B850 bacteriochlorophyll (Bchl) as; blue: B800 Bchl as; and orange: the carotenoid 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 apoprotein b-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 are labeled. The Chl a and b molecules are in red and green, respectively. Orange: the carotenoids; blue: lipids.

produce reducing equivalents that are reducing enough to be used to synthesize the fuel. In photosynthesis this requires the involvement of two separate reaction centers. Will an articial system also need two charge separation steps? The answer is, again, not yet clear. Photosynthetic light-harvesting systems consist of large supramolecular arrays of antenna complexes. These arrays self-assemble and are sometimes highly ordered but sometimes less so. A challenge for articial antenna systems is to progress from individual functional units to large arrays of these units whilst retaining efcient energy transfer to the required traps. As yet, most of the articial antenna mimics have not been organized into the large arrays that will be needed for any serious scalable device. Interesting work is being done in this area using natural antenna complexes from purple bacteria, tagging them with cysteine residues and using these to attach to ordered arrays of gold atoms on surfaces [17] . This approach could also be applied to articial antenna molecules if they too

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A Zn h

B R R NH N N NH HN

NH

NH

R R

N N

NH

Zn

H2

Zn

NH R

NH R

N R Zn NH N NH R R NH HN R
1

N R N NH R R NH NH R NH

O R=

RO

R O OR
1

R O OR
1

OR

R1 =

Figure 3. Examples of artificial antenna complexes. (A) An antenna-mimic molecule based on a small, covalently linked network of porphyrins. 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 modified with p-conjugated oligo( p -phenylene vinylene)s [57]. (C) A more elaborate attempt to produce an antenna mimic based on the LH2 structure from purple bacteria. In this case, a calix arenoporphyrin, which dimerizes to give the molecular structure depicted in this figure, has been designed to produce a model of the tightly coupled bacteriochlorophylls seen in LH2. Figures (A) and (B) reproduced with permission from [56].

are tagged. Furthermore, the assembly of articial systems under nonequilibrium conditions, possibly those of high light ux, may possibly offer an interesting route for the assembly of more efcient and functional systems. It is important to ask at this time whether light-harvesting systems are actually required for efcient photosynthesis, either natural or articial, or indeed whether they could even be detrimental. For many plants, too much light rather than too little light seems to be the problem. At light intensities much below those of full sunlight, the rate of photosynthesis saturates and the excess light energy is mainly dissipated by nonphotochemical quenching. As a consequence, research is now being conducted to see if photosynthesis can be more efcient at high light intensities if the size of the antenna

system is reduced. At subsaturating light intensities of course the case for light-harvesting complexes is clear. If the efciency of the conversion of total incident light energy into fuel is important, as we have suggested above, then light harvesting is also important in order to be able to absorb a wider range of incident wavelengths. Interestingly, Grtzel is trying to increase the overall efciency of his solar cell by including antenna pigments in order to try to absorb photons over a larger range of wavelengths (personal communication). The issue of light-harvesting capacity is therefore complicated and what is an optimal size for each reaction center will depend upon many different factors, including how fast the downstream reactions can cope with the output of the reaction centers.

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The charge-separation step

A comparison of the x-ray crystal structures of the different types of reaction centers reveals that they are very homologous (Figure4) . Moreover, the organization of the different redox components in them is, essentially, the same. This reects the fact that the structural requirements for efcient unidirectional electron transfer are very strict. Each reaction center contains a short chain of redox carriers that are arranged such that the edge-toedge distances between them in the different types of reaction centers are almost identical. These chains are required to ensure a stable charge separation and prevent energy-wasting back reactions. In reaction centers from the purple bacterium Rhodobacter sphaeroides, for example, with each forward step along the chain, the back reaction is slowed down by three orders of magnitude[18] . In photosystem II and the purple bacterial reaction centers the electron transport only goes down one of the two arms. By contrast, in photosystem I both arms are active. Very recently, it has been suggested that this may reduce the driving force required [19] . If this proves to be true then modied reaction center mimics with more than one electron transfer arm should be tested. There have been many reaction center mimics synthesized [20] . A typical example of these is given in Figure5. It is possible to make single donor-acceptor systems that show light-induced charge separation but, in these simple pairs, the back charge recombination rate is always very high and the charge-separated state is, therefore, too short to allow it to be used efciently. Inclusion of extra donors and acceptors, as seen in the natural photosynthetic system, stabilizes the charge separation so that the separated charges can now be used productively. This stabilization does, of course, reduce the redox potential available for subsequent chemical work. So far, most of these reaction center mimics can
B A Fe2+ QA HA BA P B2 A1 QA A3 BB FA

only undergo a single charge separaKey term tion event. Oxygen evolution from Water splitting: The key reaction water and the reductive chemistry whereby photosynthesis is able to extract electrons from water that are needed to make a fuel require the ultimately used to reduce carbon accumulation of multiple charges. dioxide to carbohydrate. Strategies about how to construct reaction center analogs that have multiple turnover cycles coupled with the capacity to store several charges at once are only recently being considered. Photosystem II uses a manganese cluster to store the four positive charges that result from the four single, one photon-induced turnovers that are needed to oxidize one molecule of water (Figure6) [21,22] . Unfortunately, the exact molecular details of the water splitting reaction remain to be elucidated. This problem is, perhaps, the major unsolved mystery in photosynthesis. Devising light-driven charge separation devices that are able to couple one-electron turnover reactions to chemical reactions requiring multiple charges is a major current barrier in solar fuel-based articial photosynthesis research. It would be a major breakthrough if it proves possible to couple these reactions to photoelectrochemical systems such as solar cells.
Catalysis: water splitting & synthesis of a fuel

Photosynthetic organisms have evolved to split water to release reducing equivalents. The rst step of this extremely intricate chain of chemical reactions occurs on the donor side of photosystem II. Recent advances in the structural determination of the active site of this enzyme have conrmed the presence of a manganese-oxo cluster along with some other elements in close proximity [21,22] . The cluster, together with surrounding species, is known as the oxygen-evolving center (OEC) (Figure7) . The role of the other elements (Ca2+ and Cl-) is still much debated. However, it has been known for a number of
FB C CarD1 QA PheoD1 FX QB B3 A2 ChizD1 ChlD1 TyrZ ChlD2 PD1 PD2 TyrD Fe2+ QB PheoD2 CarD2 ChizD2 Cyt b-559

QB

HB Car

Mn4Ca cluster Cyt b-550

B1

Figure 4. Comparison of the component co-factors of the electron transport chain with the polypeptide removed in the reaction center. 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].

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A H39C16 N H39C16 N N O N H17C8 O O H17C8 C8H17 O O N O N N N C16H39 C16H39 C8H17

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

years that the OEC is rstly oxidized in a series of oneelectron steps. This oxidized complex splits the water into molecular oxygen, protons and reducing power in the form of electrons. This sequence of events is known as the Kok cycle (Figure6) [23] . The OEC overcomes the two main challenges of the water oxidation process. First, it is capable of storing and utilizing the oxidative h h h h S3 S0 S1 S4 S2 power required to overcome the high thermodynamic barrier + O2 + 4H 2H2O for water oxidation. Second, Figure 6. The Kok cycle [23]. it provides a

mechanistic pathway for the simultaneous breaking of four hydrogen-oxygen bonds and the formation of the two oxygenoxygen bonds (Equation1) . This is achieved at a rate of six orders of magnitude higher than the best articial water oxidation catalyst [24] . Half reaction and potential for water oxidation: 2H2OO2+4H++4eE=1.229 - 0.059pH(25C)
Equation1

If hydrogen is the desired fuel, then it is reasonable to ask whether systems just based on the electrolysis of water could be used to split water? Conventional solar cells could then be employed to drive this process. Unfortunately, there are, at present, signicant problems that make this approach nonoptimal. In theory, the

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minimum electric potential required to split water into oxygen and hydrogen is -1.23V, under standard conditions of 25C and pH7.0. In practice, there is a large overpotential, usually between 0.5 and 0.7V. This overpotential can be reduced with the use of noble metal catalysts. Current systems for using photovoltaic solar cells to split water, and so produce hydrogen, are both inefcient and expensive, especially when compared with producing hydrogen by steam reforming of natural gas. There is a great deal of research going on to try to nd better catalysts for water splitting [2427] . If this process is ever going to be scalable at the level required to make a major contribution to the worlds energy needs, then these catalysts will have to involve the use of non-noble metals. There is, for example, not enough platinum in the world to allow it to be used in any really large-scale process for water splitting. Photosynthesis has overcome this problem by using abundant cheap metals as catalysts for water splitting. Any sensible system for articial photosynthesis must do likewise and employ common elements, such as manganese or iron. Readers interested in getting more information on this point should visit [106] , where the Center for Chemical Innovation-SOLAR project, directed by Harry Gray, is described. This is one of their major aims. As water oxidation involves a multielectron transfer process, the water splitting catalysts invariably include a transition metal in their structures. They can be differentiated in terms of their mode of action (homogeneous vs heterogeneous) and also according to the kind of ligands coordinating the redox-active transition metal (organic vs inorganic) or their bonding pattern (framework vs molecular). The design of homogeneous catalysts is more amenable to approaches that provide insights into the reaction mechanism. These types of catalysts, therefore, are easier to develop by building on information gained from spectro scopic, kinetic and theoretical ana lysis of the natural system. On the other hand, heterogeneous catalysts are generally more robust towards oxidative degradation and easier and more economical to fabricate [28] . Moreover, heterogeneous catalysts can be integrated more easily into devices that are able to couple the water oxidation process to proton reduction (and so achieve the splitting of water into molecular oxygen and hydrogen). See Brimblecombeetal. for an example of this [29] . One special class of materials that have a great deal of potential for use as both homogenous and heterogenous catalysts for water splitting are based upon a class of materials called polyoxometalates (POMs). Table1 shows the structures and main features of some molecular catalysts for water oxidation from the more well-known organometallic systems to POMs [24] . POM-based catalysts,

have recently Glu 189 burst onto the scene and made Ala 344 Ca signif icant Asp 170 O improvements Mn O O Mn in terms of rate Asp 342 Mn and turnover Mn [28,3032] . POMs O Glu 354 Glu 333 are metaloxyHis 332 gen anion clusters that have given rise to a Figure 7. Oxygen-evolving center in photosystem II. great deal of Reproduced with permission from [62]. excitement due to their oxidative stability, solubility properties and electronic tuneability. All these features suggest that this new class of water oxidation catalysts could revolutionize the eld. In this respect, many groups, including our own, are currently investigating these systems, and attempting to design new catalytically active clusters. To do this effectively requires a degree of structural control. Their structures were traditionally described as an assembly of (MOx) units where M=Mo, W, V and Nb, andx=47. Recent discoveries have expanded the POM family to clusters including noble metals such as Au and Pd [33,34] . Research in the eld is growing almost exponentially, owing to the wide range of physical properties, topologies and sizes of these types of clusters. A number of reviews have been published in the last few years that give an excellent account of their properties and applications [3537] . Polyoxometalates can be separated into heteropolyanions and isopolyanions. Heteropolyanions posses a central anion, such as SO42- or PO43-, which is thought to template the assembly of the POM in solution. Isopolyanions lack this core anion/atom. The two most important structural types within the heteropolyanions are the stable Keggin [XM12O40 ]n- and WellsDawson [X 2M18O62 ] n- anions (where M=W or Mo and x is a tetrahedral template) [36] . Lacunary heteropolyanions derive from these through the loss of one or more of the metal atoms along with the unshared O2- ligands, usually upon treatment with base [38] . They are ideal inorganic ligands as they readily coordinate other metal centers in order to ll these vacancies and, hence, regain the stability of the parent structure. When the coordinated species is a transition metal they are know as transition metal-substituted p olyoxometalates (TMSPs). One of the most successful lacuKey term nary POMs, in terms of the number of new structures obtained by using Polyoxometalates: Clusters of metal oxygen units usually containing it as a synthetic precursor, is the polyhigh-oxidation state metals Mo, W, or V 8oxoanion [SiW10O36 ] [(SiW10 )].

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Table1. Selected examples of molecular catalysts for water oxidation.

Catalyst (homogeneous) Initial turnover frequency (x10 -3 s-1) 10.0 Turnover Sacrificial oxidant number (mol O2/mol cat) 13.2 Ce(IV) Ref.

Meyer, 1982

[63]

[(bpy)2(H2O)RuORu(H2O)(bpy)2]4+ Llobet, 2004

25.9

18

Ce(IV)

[64]

[Ru2(-OAc)(bpp)(trpy)2]2+ Thummel, 2005

0.1

3200

Ce(IV)

[65,66]

trans,trans-[Ru2(-Cl)(-binapypyr)(4-Me-py)4]3+ Bernhard, 2007

7.54

2500

Ce(IV)

[66]

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

The key to this success is the fact that (SiW10) is metastable in solution [39] . This results in a range of other lacunary species related to (SiW10 ) by isomerization and/or gain or loss of tungsten-oxo units. Some of these molecules can also coordinate other transition metals in solution giving rise to a fantastic structural variety. The synthetic procedures employed to produce TMSPs are rather diverse. In the case of one-pot reactions in aqueous solution, control of certain key variables determines the structure of the product.

Using this approach we have been able to encapsulate Mn-cubanes of similar architectures found in photosystem II, into POM oxide shells. For example, a POM ligand system derived from the tri-vacant lacunary (B- a -X I V W V I 9 O 34 ) 10 - polyanion. The resulting clusters contain a central, mixed-valence (Mn 6 ) = [Mn III4 Mn II 2O 4 (H 2O) 4 ] 8+ cluster core that is anchored between two rigid lacunary [XW9O34]10- POM clusters [40] . These species were isolated as Na4K(C 4H10NO) 7([GeW9O34 ] 2

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Table1. Selected examples of molecular catalysts for water oxidation (cont.).

Catalyst (homogeneous) Initial turnover frequency (x 10 -3 s-1) 900 Turnover Sacrificial oxidant number (mol O2/mol cat) >1500 Ce(IV) Ref.

Crabtree, 2009

[67]

Cp*Xlr N 1a, X = Cl

Hill/Bonchio, 2008

37.0

385

[Ru(bpy)3]3+

[31,32]

(Ru4)(SiW10)2 Hill, 2010

130

120

[Ru(bpy)3]3+

[68]

(Ru4)(PW10)2 Hill, 2010

5000

1000

[Ru(bpy)3]3+

[28]

(Co4)(PW9)2

[Mn III4 Mn II 2O 4 (H 2O) 4 ]) see Figure 8 . Their ability to catalyze the oxidation of water is currently beingassessed. Nocera has recently reported on the insitu formation of an oxygen-evolving catalyst upon anodic polarization of an inert electrode in phosphate-buffered water containing cobalt (II) ions [41] . A dark coating forms on the surface of an indium-tin oxide electrode after electrolysis at 1.29V in a neutral KPi electrolyte (potassium phosphate pH 7) containing 0.5mM Co2+. The composition

of this electrodeposited material was analyzed using different experimental techniques. First, energy-dispersive x-ray ana lysis spectra were obtained and identied Co, P, K and O as the principal elemental components of the material. Electrolysis using large indium-tin oxide electrodes allowed microanalytical elemental ana lysis of the material and results indicated roughly a 2:1:1 ratio for Co:P:K. Finally, x-ray photoelectron spectroscopy was used to analyze the surface of the electrodeposited material. The analytical results combined indicate that

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Figure8. Representation of the polyoxometalates [{XW9}2{Mn6}]12-. The polyoxotungstate fragments are shown as polyhedra, with the central {Mn6O4(OH2)4} double-cubane cluster and the connecting heteroatoms shown as ball-and-stick (MnIII: blue; MnII: violet; X: purple; O: red; H2O = pink, H omitted for clarity).

the electrolysis of a Co2+ solution in neutral KPi solution results in the electrodeposition of an amorphous Co oxide or hydroxide incorporating a substantial amount of phosphate anion at a stoichiometric ratio of roughly 2:1:1 for Co:P:K. The Faradiac efciency of the catalyst was measured with a uorescence-based O2 sensor. After initiating electrolysis at 1.29V, the percentage of O2 corresponded to the assumption that all of the current was caused by 4e- oxidation of water to produce O2. The amount of O2 generated (95M, 3.0mg) greatly exceeds the amount of catalyst (~ 0.2mg), which shows no sign of decomposition during the course of the experiment. The insitu formation of this catalyst is unstable towards dissolution so a self-repair mechanism is implied. This involves a dynamic equilibrium set up between Co2+ HPO42- in solution and Co3+ HPO42-. This catalyst, reported by Nocera, has many elements corresponding to natural photosynthesis: its formation from earth-abundant materials, a self-repair pathway, a proton carrier in neutral water and ability to generate O2 at low overpotential, neutral pH, 1atm and room temperature. It will be interesting to see if Noceras approach can be incorporated into a cheap, scalable device powered by solar energy that can allow the often discussed hydrogen economy to become a reality. It is beyond the scope of this short review to discuss the major issues involved in the storage and use of hydrogen as an energy source. Although it is not a liquid fuel, hydrogen is an example of a fuel that is currently being made as a solar fuel. In such systems, hydrogen can be made by the reduction of protons using the enzyme hydrogenase [42] . A great deal of both structural and functional information is available on this enzyme [4346] . As a consequence, there is currently a

great deal of effort trying to test the feasibility of using it, both invivo in algal bioreactors and in various biohybid systems, to produce hydrogen. This type of endeavor is the main aim of the Solar-H consortium, which is a panEuropean research group [107] . One of the major drawbacks of using hydrogenases is that they are very oxygen sensitive [42] . There are, however, some small bacterial hydrogenases that are more oxygen tolerant that hold out the possibility of being able to solve this problem. Many hydrogenases, however, operate with an equilibrium constant of 1. This means that any signicant build up of hydrogen will act back on the reaction and inhibit it. This has big implications for how the evolved hydrogen can be collected. Nitrogenase can also act as a hydrogenase in the absence of nitrogen, and because its reaction is very exothermic, it can produce hydrogen against backpressures of several atmospheres [47] . Unfortunately, it is even more oxygen sensitive than hydrogenase and has a large energy requirement. An ideal solar fuel would be one where atmospheric carbon dioxide could be reduced to produce it. This would then set up a sustainable recycling of carbon dioxide with it being removed from the atmosphere to form the fuel and then produced again during the fuels combustion. This, of course, is what photosynthesis does, although in this case the fuel produced carbohydrate is not sufciently reducing to be used directly as fuel for transport, for example. At present there are no catalytic systems available that can convert atmospheric carbon dioxide into a hydrocarbon suitable for use as a fuel for transportation. It is possible, however, to use formate dehydrogenase running in reverse together with alcohol dehydrogenase, and convert carbon dioxide into methanol [48,49] . The reduction of carbon dioxide to formate has been driven by light using a p-type indium phosphide solar cell and the enzymatic reactions involved have been shown to be enhanced when they are encapsulated in silica sol-gel matrices. Formate dehydrogenase can be coupled to electrodes and then the reverse reaction can be driven by the voltage from the electrode [50] . It will be interesting to see if these enzymes can be linked into a practical device for making solar fuels. Very recently, there has been a report of a cell-free articial photosynthesis system set up in a ranaspumin-2 based foam [51] . This foam is produced by some Tungara frogs such as Physalaemus pustulosus. Bacteriorhopsin and a thermophilic ATP synthetase were inserted into lipid vesicles formed from the ranaspumin-2 surfactant protein isolated from the frog. Some of the Calvin cycle enzymes, riblulose-1-5 bis-phosphate and NADPH were added to the compartments formed by the foam and light-driven carbon dioxide xation into glyceraldehyde3-phosphate was seen. This is an interesting system, not because it is likely to be scalable to make large amounts

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of solar fuel but because it highlights the importance of compartmentalization. Photosynthesis relies upon this and it is highly probable that compartmentalization will also be required to be part of the design of any practical articial system capable of producing solar fuels. Future perspective Articial photosynthesis holds out the promise of being able to provide an efcient way of producing solar fuels. As outlined above, using the conceptual framework of breaking down photosynthesis into its four general steps provides a focused way to attack the problem of making robust systems for replicating each of these stages. Currently, the most challenging bottlenecks to the achievement of even microscale systems for solar fuel production based on articial photosynthesis are the catalytic steps needed for water oxidation and fuel production. We are not daunted by these problems. Rather, we are encouraged since more and more talented researchers are now rising to this challenge. We expect that during the next 10years, the crystallography of photosystem II will be greatly improved. As a result of this the structure of the OEC will be determined to high resolution in each of the different S states. This will reveal the secrets of the precise mechanism of the water splitting reaction. The role of the protein will then be precisely determined. This will provide the blueprint for synthetic chemists to design a new generation of catalysts that will place the mimic of the OEC into a smart matrix that will truly r eplicate the catalytic power of the natural system. Biology has evolved by changing the matrix (the protein) and this is why enzymes are such remarkable catalysts. Biology uses self-assembly and self-repair to produce long-term stability in processes such as photosynthesis.
Executive summary

Articial photosynthesis will also probably need to use these techniques if it is to become scalable. This idea has been considered before but has not yet become a serious research focus. We expect this will change rapidly in the next few years. Processes such as water splitting involve highly dangerous oxidizing species. Self-repair will therefore be important to build into any device that splits water and is required to have a long lifetime (namely, years). Many of the enzymes that can be harnessed to produce fuels, such as hydrogenase or nitrogenise, are currently very oxygen sensitive. We expect the molecular details of this oxygen sensitivity will be elucidated and modied enzymes capable of producing hydrogen in the presence of oxygen will be produced. Most probably thermophilic varieties of these enzymes will be used as they will have enhanced stability. We expect that during the next 10years, small demonstration systems will be constructed based on articial photosynthesis that can make solar fuels. Research in this area is at a fascinating stage. We know what we want to achieve. We know the end point we want to reach. What we do not yet know, is how to get there. However, since biology obeys the same rules of physics and chemistry, as all other processes on earth, if we have sufcient insight into the biological process then it must be possible to replicate it. This rationale provides the hope not only for this area of research, but for our future on this planet. One of the grand challenges mankind faces is to devise ways for the sustainable production of carbon-neutral fuels. The benets for addressing climate change is clear, this approach could give rise to a technology that would take the fossil out of the fuel, allowing real-time recycling of carbon dioxide, negating the need to access harder-toextract and dirtier forms of fossil fuel for when oil and gas run out.

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 surface area required for light harvesting.

There is often confusion with the definition 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 artificial photosynthesis for producing solar fuels can be constructed by analyzing each of these
four partial reactions.

Recent progress in determining structural function of the photosynthetic pigment protein complexes responsible for carrying out light
harvesting and charge separation have informed the design of artificial mimics of both of these steps in the photosynthetic process.

The major hurdles to be overcome in achieving artificial photosynthesis are producing catalysts capable of splitting water and reductive
synthesis of fuels.

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

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.

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Financial & competing interests disclosure

Tatas Brotosudarmo gratefully acknowledges nancial support from the United States Department of Energy, DOE Energy Frontier Research Center (DE-SC0001035). Leroy Cronin and Richard Cogdell thanks the EPSRC for funding and Leroy Cronin for the award of Royal Society-Wolfson Foundation award. The authors

have no other relevant afliations or nancial involvement with any organization or entity with a nancial interest in or nancial conict with the subject matter or materials discussed in the manuscript apart from those disclosed. No writing assistance was utilized in the p r oduction of this manuscript.
22 Guskov A, Kern J, Gabdulkhakov A, etal.

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Review Cogdell, Brotosudarmo, Gardiner, Sanchez &Cronin

68 Besson C, Huang Z, Geletii YV etal. 102 California Institute of Technology, LEWIS

Cs9[([g]-PW10O36)2Ru4O5(OH)(H2O)4], a new all-inorganic, soluble catalyst for the efcient visible-light-driven oxidation of water. Chem. Commun. 46, 27842786 (2010).

research group. Global energy perspective. http://nsl.caltech.edu/energy

103 Energy Biosciences Institute.

www.energybiosciencesinstitute.org
104 US Department of Energy Ofce of Science.

Shows the ESF report on solar fuels, with particular emphasis on the role of photosynthesis. The possible uses of both natural photosynthetic systems and articial bio-inspired ones are discussed. www.ccisolar.caltech.edu

Websites
101 Basic research needs for solar energy utilisation

106 Center for Chemical Innovation. 107 Uppsala University, Department of

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

Genomic science program. http://genomicscience.energy.gov/centers/ index.shtml

105 European Science Foundation (EFS).

Shows the major Department of Energy report on possible ways to harness solar energy. It provides a comprehensive state of the art picture of research in this area.

Harnessing solar energy for the production of clean fuel. www.esf.org/publications/science-policybriengs.html

Photochemistry and Molecular Science. www.fotomol.uu.se/Forskning/Biomimetics/ solarh

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Biofuels (2010) 1(6)

future science group