Artificial photosynthesis

We raise here a series of critical issues regarding artificial photosynthesis with the intention of increasing awareness about what needs to be done to bring about a working prototype. Factors under consideration include energy and electron transfers, coupled redox reactions, repair mechanisms, and integrated photosystems.
Andrew C. Benniston and Anthony Harriman* Molecular Photonics Laboratory, School of Chemistry, Bedson Building, Newcastle University, Newcastle upon Tyne NE1 7RU, UK *E-mail: anthony.harriman@ncl.ac.uk

Natural photosynthesis, the process whereby CO2 is converted into carbohydrate and water is oxidized to molecular oxygen, has supplied the overwhelming majority of stored energy available on our planet1. This stored energy, which is mostly in the form of fossil fuels, had sufficed for billions of years and it is only very recently that the stocks of fuel have started to deplete at a rate faster than Nature can replenish2,3. Indeed, our insatiable appetite for instant energy is set to expand at an unprecedented pace and our capability to generate CO2 knows no bounds. The need to provide additional energy and to deal with the ensuing ecological problems associated with current lifestyles in the developed world pose tremendous challenges for the scientific community4. The urgency, and therefore the funding, devoted to solving these problems is set exclusively by the price of oil and, as a consequence, the attention given to meeting these challenges is driven by market forces. Once again we are entering a period of wildly fluctuating oil prices and this time, unlike the 1970s, it is unlikely that the cost per barrel will fall steeply after an uncomfortable ride. The search for renewable energy supplies is now a major issue for all stable governments but it must be accompanied by new initiatives to reduce CO2 levels and, in as much as it is possible, sequester CO2 from the atmosphere. This is

precisely how photosynthesis works and although many intriguing alternatives merit consideration at a local level, it is crucial that scientists are given the opportunity to produce a viable form of artificial photosynthesis. The overall challenge is massive and needs to be addressed by a multinational force dedicated to the task it is far beyond the capability of a single investigator. Most of the chemistry associated with natural photosynthesis is understood at a reasonably precise level5. The reagents, chemical reactions, rates, and mechanisms have been known for decades6,7 and although refinements continue to be made, the basic understanding is in place8. Likewise, the structure and level of organization of the essential features of photosynthesis have been elucidated by biophysicists and further defined by protein crystallography (a full compendium of X-ray-determined structures of membrane proteins can be found at http://www.mpibp-frankfurt.mpg.de/michel/public/ memprotstruct.html) and advanced theory9. How can we utilize this information to engineer an artificial leaf? This is the key question and the answer is that no one knows. We can, however, set out the state of current knowledge and thereby expose the main challenges that remain. In so doing, we emphasize the underlying chemistry. Our rationale for this approach is that we need first to devise suitable chemical processes before attempting to build working prototypes. The

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engineering principles, daunting in themselves, need to be developed once the chemistry is in place.

The first artificial photon collectors comprised covalently linked porphyrin dimers that displayed highly efficient excitation energy transfer over short distances16. These were followed by detailed studies of clusters, arrays, dendrimers, and polymers. More recently, extremely long, porphyrin-based ribbons have been reported17 and attempts have been made to develop porphyrin-based wheels and rings18. In all cases, electronic energy transfer is fast and highly efficient. There is, however, an additional requirement in that energy produced following excitation must percolate through the system to terminate preferably on a single chromophore19. By ensuring that an energy gradient is set up within a molecular system, this cascade effect is readily achievable but does require careful design and choice of chromophores. A fine example of this is the molecular array shown in Fig. 220, which comprises four different, yet complementary, organic chromophores. The color code attempts to show the internal energy gradient in that the fluorene molecule (blue) absorbs high-energy photons and the bodipy (red) is the terminus. The arrows show the pathways for energy migration depending on which chromophore is illuminated. It is worth noting that essentially all absorbed photons terminate at the bodipy unit. The natural system is highly ordered but this is not true for most artificial prototypes, despite their synthetic attractiveness. The first attempts to create ordered networks for electronic energy transfer were described by Mobius and Kuhn21 and involved monomolecular layers of cyanine dyes coated onto transparent slides. Other reports have focussed on energy transfer in polymeric media, leading to the development of solar concentrators of the type illustrated in Fig. 322.

Capturing the photons

Sunshine is diffuse and although sufficient sunlight reaches the surface of the Earth to satisfy all our energy needs, it must be concentrated at some stage in the overall storage process. Nature accomplishes this essential task by using light-harvesting complexes to collect incident photons, move them over large distances and direct them to a site where the chemistry takes place10. The light-harvesting complex is a highly organized array of chlorophyll molecules as illustrated in Fig. 111. Many such arrays act cooperatively both to shuttle photons to the right place and to avoid the problems of overload at high light intensity. The structural elegance and chemical efficacy of the natural system have stimulated great interest in artificial analogs, mostly involving porphyrin-based chromophores12. Nature has opted to transfer excitation energy between weakly coupled chromophores via the so-called Frster mechanism13, which involves through-space interactions, but artificial systems tend to supplement this route with electron exchange interactions occurring within more strongly coupled chromophoric arrays14. A crucial feature of all such systems is the need to avoid involvement of triplet states, since these will inevitably transfer energy to oxygen and form the highly destructive species known as singlet molecular collector. oxygen15. This latter metastable reagent is responsible for rapid aging and ultimate destruction of the photon

(a)

(b)

Fig. 1 Representation of the X-ray structure of bacterial light-harvesting complexes. (a) Ring of 18 B850 bacteriochlorophyll-a molecules and (b) ring of nine B800 bacteriochlorophyll-a molecules with a different ring between the helices of the apoproteins. The -apoproteins are colored yellow and the -apoproteins green. Electronic energy is transferred around the ring, between cofacial pigments, in an incoherent manner until it migrates to a different ring. Eventually, the photon reaches a light-harvesting complex with a reaction center complex embedded in its center. (Reproduced by permission of McDermott et al.11.)

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Fig. 2 A tailor-made artificial light-harvesting array based on fluorene (blue), pyrene (purple), perylene (green), and bodipy (red) units. Each unit is selected for its complimentary absorption profile. Arrows depict the pathways for energy migration to the terminal unit. Note that a wide spectral range is harvested in this way, with essentially every absorbed photon being directed to the bodipy core. In this case, energy occurs by way of both through-space and through-bond processes, unlike in the natural system, as indicated in the insert.

transferring energy from the p-quaterthiophene residue (yellow) to the bodipy core. The energy-transfer rate increases six-fold when the dyad is dispersed in a soft glass. Considering that artificial systems will be required to operate in the solid state, these results are encouraging for creating models using the bodipy chromophore. Furthermore, since thiophene groups are easily polymerized, the manufacture of polymeric materials looks entirely feasible. Finally, we note the novel experiments reported by Calzaferri and coworkers24,25 using dye-loaded zeolites. Here, rationally designed dyes are either incorporated into channels inside the zeolite or used to block the pore. Energy transfer can then be directed along the channel. Quite separately, research has progressed into the design of light-harvesting units for dye-injection solar cells of the type pioneered by Grtzel26. Here, a dye sensitizer is used to inject charge into nanostructured surfaces such as fractal TiO2 in contact with a suitable redox-active electrolyte. Considerable work has gone into the optimization of the photon-collecting properties of the sensitizers2731
Fig. 3 Example of an organic solar concentrator in the form of a very low concentration of dye dispersed in a polymeric film and coated onto a glass surface. The upper panel was taken without illumination while the lower panel shows fluorescence from the thin film. Note how the fluorescence is localized at the edge.

and into engineering the cells for stable performance3235. Further attention has been paid to photon collectors for low band-gap organicbased solar cells3640 and many of the basic concepts are common to all types of light harvesters.

More recently, attention has turned to the possibility of energy transfer occurring in crystalline media. Thus, although the dyad23 shown in Fig. 4 is not as elaborate as the multichromophore systems outlined above, it operates as a photon collector in the crystalline state by

Charge separation
The light-harvesting complex directs photons to a Reaction Center Complex (RCC) where the absorbed photon is used to drive an electron-transfer reaction that leads to charge separation across a

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Fig. 4. Illustration of a bodipy-based molecular dyad used for studying intramolecular electronic energy transfer, and the crystal packing diagram of the molecules as determined by X-ray crystallography. UV photons absorbed by the oligothiophene unit are transferred efficiently to the bodipy dye, which fluoresces strongly, despite the orthogonal connection. Energy transfer becomes more efficient as the orthogonality is relaxed. Color code: S = yellow, B = orange, F = green, N = blue, C = gray. (Reproduced in part by permission of Benniston et al.23.)

biological, lipid bilayer membrane (Fig. 5)41. Nature has evolved this cascade-type effect in which the electron and positive hole move further apart through a series of short-range jumps as a means to circumvent rapid charge recombination between the electron and hole. Research into artificial analogs of the natural RCC has advanced rapidly, aided by elegant theoretical models42,43, stimulated by studies of the crystal structure of the bacterial RCC44,45, and

facilitated by tremendous advances made in our understanding of simple electron-transfer processes by pioneers such as Mataga46, Closs47, and Wasielewski48. Early work on artificial versions of the RCC used porphyrinquinone dyads but these suffered from fast charge recombination49. The essential breakthrough was made by Gust et al.50, who reported the first molecular triad, based on the realization that the rate of electron transfer decreases exponentially

Fig. 5. Spatial arrangement of the cofactors in the photosynthetic reaction center complex of the purple bacteria Rhodobacter sphaeroides, as determined by X-ray crystallography. Photons arrive at a special pair of bacteriochlorophyll molecules (green), by way of the light-harvesting complex. Electron transfer then occurs, first to the monomeric bacteriochlorophyll (blue) and subsequently to the free-base bacteriopheophytin (red), then to the first quinone (yellow, QB) and finally to the second quinone (purple, QA). There is an iron center associated with the quinone residues. By way of such a cascade of electron-transfer steps, transmembrane electron transfer is achieved. Note the symmetry of the tetrapyrrole-based cofactors, but it should be realized that electron transfer occurs exclusively along the right-hand branch. (Reproduced by permission of Dr R. Wheeler.) The insert shows how the RCC fits inside one of the light-harvesting rings.

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Fig. 6 Simplified energy-level diagram showing the principle of charge separation via sequential electron-transfer steps. Excitation leads to formation of the singletexcited state localized on the chromophore, which is also the primary donor (D1). In competition with fluorescence, charge separation occurs to form the radical ion pair in which an electron has been transferred to the primary acceptor (A1). Secondary electron transfer to form the extended radical ion pair can compete with charge recombination to reform the ground state. Provided the thermodynamics can be satisfied, hole transfer can occur to move the oxidizing equivalent to the secondary donor (D2). Charge recombination is now very slow because of the large distance separating the charges. Note that a certain fraction of the initial excitation energy is lost at each stage.

with increasing separation between the reactants. This has led to the introduction of countless triads51, tetrads52, pentads53, etc., that are loosely modeled on the architecture of the RCC but allow for the fact that there is no need to accurately duplicate all the structural facets. The basic idea is to move electrons from one side of the supermolecule to the other side as quickly and as efficiently as possible, so that the positive and negative charges become spatially remote. It is important to realize that simply making long molecules is not the answer to the charge-recombination problem and careful choice of the individual units is essential (Fig. 6). Considering the time and effort required to synthesize elaborate multicomponent molecules, the wrong design could be disastrous. Even so, some superb molecular structures have been described that closely resemble the natural RCC, often having the quinone replaced with a fullerene derivative. A great variety of molecular dyads have been synthesized in order to critically examine various aspects of electron-transfer theory. These

have included weakly associated conjugates, such as the hydrogenbonded systems reported primarily by Sessler et al.54, as well as covalent analogs. A persistent line of enquiry has been to pursue unusually long-lived charge-separated states without the need for extended synthesis. All such attempts have failed, although there have been several erroneous reports to the contrary55. This has necessitated the formulation of a set of rules that must be fulfilled in order to claim a long-lived, charge-separated state56. The advantages of such simple dyads are obvious but something rather special is needed to circumvent the inherently fast rates of charge recombination, especially when dealing with high-energy states able to form triplet species57. Unfortunately, this special ingredient has defied identification and there are many who doubt its existence! The situation is illustrated in Fig. 7. It is evident that the final design of a molecular system for artificial photosynthesis will require the coupling of the light-harvesting

Fig. 7 Simplified energy diagram showing processes that take place following illumination of a molecular dyad. Excitation results in formation of the singlet-excited state localized on the chromophore, which is also the primary electron donor. This species can fluoresce but can also transfer an electron to an appended acceptor, forming a charge-separated state. In turn, this latter species can decay via charge recombination or undergo intersystem crossing to form a triplet-excited state localized on either donor or acceptor. The triplet is liable to transfer energy to oxygen, forming the highly dangerous species, singlet molecular oxygen.

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portion to the artificial reaction center. The example shown in Fig. 858 utilizes a unique combination of zinc and free-base porphyrins and an electron-affinic C60 terminal. Selective illumination of the peripheral zinc porphyrin causes energy migration first to the central group and then to the free-base porphyrin shown in green. The resultant excited state transfers an electron to C60 in about 25 ps. The positive hole formed initially on the free-base porphyrin migrates to the zinc porphyrin under thermodynamic control to create a charge-separated state in high yield that survives for 25 s. This is sufficient time to allow useful catalytic processes to compete with long-range charge recombination. As with electronic energy transfer, the question must be posed as to how it is possible to impose directionality on the electron-transfer event. Again, the first rationale attempts to study electron transfer in organized media were made by Kuhn59, with his LangmuirBlodgett films. Modified enzymes have been prepared by several groups and employed to direct an electron from a donor on the surface to a specific site within the protein. Such experiments have led to a deeper understanding of how electrons tunnel through protein matrices60. Others have assembled molecular dyads around DNA duplexes and thereby set up one-dimensional electron-transfer pathways61. More elaborate systems have been used to pump electrons across liposomes and membranes, and in particular Gust et al.62 have been highly

successful in this field. The key puzzle, however, is how to extend such work to engineer photoactive films with oriented arrays of multicomponent supermolecules that can be printed on large surface areas and that retain the activity of isolated molecules in a polar solvent. Building ever more intricate molecular systems that closely resemble the structural features of the RCC is an interesting academic challenge but gets us no nearer to a successful artificial photosynthetic system. Some success has been achieved with self-assembled -stacks, but these lack the true element of directionality needed to drive photochemical water cleavage. At this time, artificial photosynthesis lags far behind photoelectrochemical systems, such as organic photovoltaics63,64 or dye-injection solar cells65, and it is clear that new initiatives are urgently needed.

Photocatalytic cycle
Photochemistry provides direct access to potent oxidizing or reducing species that can be used to drive redox reactions, leading to useful chemical feedstocks. There are two inherent problems to overcome. Firstly, the species generated by photolysis are the result of oneelectron transfers but formation of stable chemicals requires at least two, and often four or more, electrons. As such, some kind of charge accumulation is needed to couple the photochemical steps to product formation. Secondly, to avoid back-reactions between the

Fig. 8 Illustration of a molecular array that acts as both a photon collector and an artificial reaction center. Arrows show pathways for energy migration to the terminal free-base porphyrin, from where electron transfer to the attached C60 residue takes place. The resultant charge-separated state is susceptible to fast charge recombination, during which the excitation energy is converted into heat, but hole transfer (ht) occurs from the free-base porphyrin -radical cation to one of the appended zinc porphyrins. In this way, the charges become spatially isolated and the rate of charge recombination decreases. For the example shown, the lifetime of the charge-separated state is 25 s.

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photochemical products, it is necessary to design and subsequently link two separate cycles one forming a fuel and the other providing the all-important oxidizing agent. Using water as the electron source, for example, individual photosystems would be engineered to produce H2 and O2 but they would need to be connected via a common relay. In fact, many individual photocycles have been optimized for the generation of certain small molecules. Photochemical generation of H2 from organic substrates in the presence of a suitable electron-storage catalyst is trivial66. The catalyst can be a precious metal colloid67 or an enzyme68 and the system can be made to work extremely well; the example shown in Fig. 9 is the most advanced photosystem of this type69. It stops only when the chromophore has been fully hydrogenated or when the substrate runs out. Suitable substrates might be waste materials or glycerol left over from biofuel production. It is much more difficult to identify suitable catalysts for CO2 reduction and even more so for NH3 formation. This latter reaction would be an ideal way to generate cheap supplies of fertilizer for developing countries but there are no viable systems known at the present time. Likewise, the photooxidation of persulfate to O2 has been perfected using a range of chromophores and with colloidal RuO2 or IrO2 as catalyst70. Turnover numbers tend to be modest and the harsh experimental conditions destroy the chromophore. Prolonged attempts to replace the colloidal redox catalyst with simpler molecules able to undergo several changes in oxidation state, most notably manganese porphyrins, have not been successful71. Indeed, now that the structure of the natural O2-evolving catalyst is available7274, it is clear that there are no artificial analogs. The search for improved oxidation catalysts continues7580. Milder conditions can be used for halide oxidation and this is a viable alternative to O2 production, especially using seawater as the substrate. Producing a mixture of gaseous H2 and O2 is clearly undesirable81 and there are major problems involved in collecting H2 evolved over

a wide area. The only realistic option is to couple O2 generation with the two-electron reduction of a relay (Q) and to use the resultant QH2 as a raw material in a separate photocycle under conditions where the H2-evolving catalyst is localized at the collection point82. The overall scheme is shown as Fig. 10. Here, water is the source of the O2 and the reduced relay can be isolated, stored, and used for fuel production as required. Ideally, the second cycle would reduce CO2 to formic acid83. This product could be concentrated and used either as a feedstock or as a source of H2. Quinones are often considered as potential relays but there has been little genuine progress in effecting this type of coupled system. Even less is known about how to selectively reduce CO2 to formic acid84, although its subsequent dissociation into CO2 and H2 is well known85. We emphasize that such coupled systems represent the only viable approach to storing sunlight as chemical potential, while the need to invoke CO2 reduction has become almost as important as seeking new energy supplies. The absence of any genuinely effective catalyst for CO2 reduction remains a massive stumbling block. That is not to imply that strenuous efforts to identify suitable catalysts have not been made. On the contrary, many different approaches have been tried, but a genuinely effective catalyst for CO2 reduction remains elusive8693.

Molecular self-repair
Perhaps the most intriguing aspect of biological systems is their ability to induce self-repair. In contrast, virtually no man-made materials that have a dynamic function possess the ability to sense and repair the inevitable damage that occurs during operation. Self-repair is an essential feature of natural photosynthesis; for example, an oxygenevolving catalyst is known that can regenerate each 30 minutes under solar irradiation94 while highly reactive singlet oxygen formed during side-reactions is consumed by carotenoids95. The idea that an artificial analog built from organic molecules and maintained under

Fig. 9 Advanced photosystem for the photochemical dehydrogenation of ethanol. The photoactive ingredient is a tin(IV) porphyrin and the primary donor is NADH. This latter species is regenerated using alcohol dehydrogenase (ADH) as selective catalyst. The reduced porphyrin is used to chemically reduce methyl viologen (MV2+). This latter species is recovered in a separate catalytic process in which colloidal Pt reduces water to H2. The net reaction is the conversion of ethanol to acetaldehyde and H2 gas. The system is shown as a two-electron cycle.

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Fig. 10 Simplified representation of a two-color photosystem for solar energy conversion using a relay. S refers to a sensitizer, which might differ for each reaction, whose purpose is to absorb photons and initiate the necessary redox chemistry. Suitable catalysts are mandatory.

illumination in aerobic conditions can operate without self-protection is foolhardy. No amount of engineering will overcome this problem and it is crucial that practical photosystems are equipped with some kind of built-in protection against photochemical damage. This aspect of artificial photosynthesis is still in its infancy but four possible mechanisms can be identified: redundancy, reservoir effects, excision and replacement, and on-site repair. One such strategy is exemplified in Fig. 11, where two of the blue porphyrin arms are redundant during a complete photon cycle96. If one, or even two arms, became damaged over time the system will not necessarily shut down. Providing a repair mechanism could be put in place, the array would eventually re-establish its full working capacity. The ability to create intelligent artificial repair enzymes is of course a major challenge.

Closing remarks
Solar panels on the roof, charging a battery in the basement, are becoming commonplace. Cars powered by the electrolysis of water no longer reside solely in the world of fiction. What price power stations harnessing sunlight and turning out designer fuels for the chemical industry using water as the sole source of electrons? The photofixation of CO2, once an esoteric research dream, is now a necessity, to be utilized to create organic molecules as substitutes for fossil fuels. We have to develop new catalysts to drive these reactions under mild conditions and to integrate fundamental principles of light-induced electron transfer into ordered arrays where individual molecules act cooperatively on a large scale. The challenge is immense but so too is the reward. Complacency

(a)

(b)

(c)

Fig. 11 Illustration of artificial self-repair processes, including (a) redundancy, (b) the reservoir effect, and (c) inclusion of a bridge that could be cut out and replaced by selective chemistry at the connections. In each case, illumination of the donor results in through-bond electron transfer to the acceptor but occurs only if the linkage is intact.

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engulfs us as we talk endlessly about progress made to date in terms of efficiencies of light-to-electricity conversion. The simple reality is that little real progress has been made in artificial photosynthesis

over the past 20 years a fact dictated by the affordable price of oil. Doubts are being raised as to whether we have a further 20 years to waste.

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