What Can We Learn from Photosynthesis About How to Convert Solar Energy into Fuels

Richard J. Cogdell, Katsunori Nakagawa, Masaharu Kondo, Mamoru Nango, and Hideki Hashimoto

Abstract We briefly review the need for construction of novel systems for the production of clean renewable fuels to replace oil and gas. Then the case is made that if it will be possible to gain a sufficient understanding of photosynthesis that it should be possible to use this information to produce "artificial leaves". These artificial leaves will be designed to convert solar energy into dense portable fuel.

Keywords Solar fuels • Photosynthesis • Artificial leaf • Global warming

1 Introduction

Currently in the developed world we get our energy mainly from fossil fuels. In fact approximately 70-80% of our current energy needs are met by burning coal, oil and gas. Unfortunately oil and gas supplies are predicted to be largely exhausted by the end of this century. Also we have a major problem caused by the increasing rates at which we currently consume fossil fuels, namely global warming caused by elevated levels of CO2 in the atmosphere. As a result of these two imperatives there is an urgent need to develop new, clean, scalable, and renewable sources of fuels. Providing for our requirements for electricity is not such a fundamental problem. There are many clean and renewable energy sources that can be used to produce electricity, e.g. wind, solar energy, hydro, thermal, etc. The main challenge is to

University of Glasgow, Glasgow G12 8TA, Scotland, UK e-mail: [email protected]

Nagoya Institute of Technology, Gokiso-cho, Showa-ku, Nagoya, 466-8555, Japan

K. Nakagawa, M. Kondo, M. Nango and H. Hashimoto CREST/JST, Saitama, Japan

H. Hashimoto

Osaka City University, 3-3-138 Sugimoto, Sumiyoshi-ku, Osaka 558-8585, Japan find ways of producing clean sources for the production of dense portable fuel. If the aeroplanes are to be kept in the sky and the ships are to be kept at sea, then a fuel equivalent to gasoline will be required.

One possible abundant energy source that in principle could be harnessed to produce fuel is the sun. More than enough solar energy reaches the surface of earth each hour to satisfy all our current energy requirement for one year. How can we use this plentiful supply of solar energy to produce fuels? There is already a process that takes place on our planet that converts solar energy into fuel. This process is photosynthesis.

2 What Is Photosynthesis?

Photosynthesis is the process whereby plants, algae, and some bacteria are able to use solar energy to convert atmospheric carbon dioxide into sugar (a fuel). Indeed all the fossil fuels that man is currently so greedily consuming represent photosyn-thetic activity that occurred in the past millennia. If we could fully understand photosynthesis would it be possible to use this knowledge to produce robust, efficient artificial systems to convert solar energy into fuels. Although, at present we do not have all the detailed information that is needed in order to produce such systems it is possible from a consideration of the essence of photosynthesis to start a long the path towards succeeding in this aim.

Photosynthesis can be divided into four key partial reactions [1]. These are light-harvesting (light-concentration), using this concentrated light-energy to separate charge across a membrane, accumulation of positive charges on one side of this membrane in order to extract electrons from water (water splitting) and accumulation of the negative charges on the other side of this membrane in order to do catalysis to produce a fuel (e.g. the conversion of carbon dioxide to carbohydrate) (Fig. 1).

Fig. 1 A representation of the four key partial reactions of photosynthesis

Fig. 1 A representation of the four key partial reactions of photosynthesis

3 Concept of the Artificial Leaf

Jim Barber from Imperial College in London has championed the idea of an artificial leaf. This is an elegant concept that really clearly illustrates the idea of using the photosynthetic blueprint in order to design ways of using solar energy to produce fuels. We will now consider each of the four key partial reactions of photosynthesis, outlined above, in order to assess where current research is along path to producing fuels from solar energy. We will describe both current approaches and where we think the major bottlenecks are.

Solar energy, though an abundant energy source, is a diffuse low-density energy source. This means that relatively large surface areas are required to harvest and concentrate this energy before it can be used to make fuel. Photosynthesis achieves this through its light-harvesting pigment-protein complexes. We are now in the fortunate position of having several high-resolution X-ray crystal structures of light-harvesting complexes from a variety of different photosynthetic organisms. It is possible therefore to ask whether there are some key common design features that can be found in these structures (Fig. 2).

Remarkably the structures of antenna complexes from different species are found to be highly variable. Initially it might be thought that this is a very disappointing result. Why should these structures be so variable? The answer is that the

Fig. 2 Examples of the X-ray crystal structures of different light-harvesting complexes. (a) LHCII from higher plants [2], (b) peridinin-chlorophyll a protein from dinoflagellates [3], and (c) LH2 complex from two different species of purple bacteria [4, 5]

physics of energy-transfer is very tolerant. So long as the light-absorbing pigments are arranged close enough singlet-singlet energy-transfer will remain efficient even when the positioning of these pigments is quite variable. This design tolerance rather than being disappointing is encouraging to researchers who are trying to construct artificial systems designed to replicate biological light-harvesting. It means that there will be many different potentially successful ways of constructing light-harvesting modules [6].

Photosynthesis uses reaction centres to drive a transmembrane charge separation process powered by light energy provided by the light-harvesting system. Again there are several high-resolution X-ray crystal structures of photosynthetic reaction centres from several different species of photosynthetic organisms. In this case the basic structure of these reaction centres and organization of the redox centres within them is very highly conserved [6] (Fig. 3).

In contrast to energy-transfer the structural constraints on electron transfer are much more stringent. Even though this is true several artificial analogues of the basic reaction centre structure have been synthesized and shown to successfully separate change upon illumination. It appears therefore that it is not too difficult to construct artificial systems that can successfully mimic both light-harvesting and charge-separation.

At present the major bottlenecks both conceptually and practically are where the one electron redox reactions characteristic of a basic reaction centre interface with the chemical reactions that require either multiple positive or negative charges. The reaction centre of photosystem II also houses the water splitting apparatus.

Fig. 3 Structure of the purple bacterial reaction centre and a view of the organization of the reaction centre redox carriers with the protein subunits removed (PDB: 1RGN). P is the special pair of bacteriochlorophyll molecules that go oxidized upon illumination. B is a monomelic bacteriochlo-rophyll. H is a bacteriopheophytin molecule. Q is a quinone. Charge is separated down the A branch and the negative charges are accumulated by QB

Fig. 3 Structure of the purple bacterial reaction centre and a view of the organization of the reaction centre redox carriers with the protein subunits removed (PDB: 1RGN). P is the special pair of bacteriochlorophyll molecules that go oxidized upon illumination. B is a monomelic bacteriochlo-rophyll. H is a bacteriopheophytin molecule. Q is a quinone. Charge is separated down the A branch and the negative charges are accumulated by QB

Unfortunately the X-ray crystal structure in this area only reveals an outline of the catalytic centre that is capable of storing four positive charges and then using them in a concerted reaction to split water into oxygen, protons and electrons (Fig. 4).

What is needed is structures of this catalytic centre in each of its individual redox states together with a detailed understanding of how the protein in the region of manganese centre participates in the reaction mechanism. There have been numerous attempts to mimic the structure of the water splitting centre with just the manganese/calcium/oxygen atoms [e.g. 8]. None of these metal complexes are able to reproduce the catalytic power of the natural system. We expect that this will remain to be the case until models include the function of the protein (a smart matrix) as well as just the ion centre. A similar barrier to progress exists on the side of the negative charges. There are however enzymes that are able to store negative charges in order to do a catalytic reaction required to produce fuels. The simplest

4 hv

Fig. 4 The overall structure of photosystem II together with the picture of the water splitting centre [7]

example of such enzyme is hydrogenase [9]. This enzyme is able to reduce protons to produce hydrogen. Although hydrogen is not very dense fuel, there are many situations in which it could usefully substitute for denser carbon based fuels. Hydrogenase does provide a useful model system with which to develop the methodology to couple the reaction centre to an output capable of producing fuel. Unfortunately most hydrogenases are very oxygen sensitive. They are inactivated in the presence of oxygen. This is a major problem, since on the other side of the reaction centre oxygen is going to be produced. Recently hydrogenases have been found in anaerobic purple photosynthetic bacteria that are much less oxygen sensitive. It is to be hoped that when the details of the origin of this oxygen insensitivity are understood that hydrogenases resistant to oxygen can be incorporated into devices designed to be artificial leaves.

4 Outlook for the Future

Photosynthesis is a subject to the same laws of chemistry and physics as every other process on earth is. There is nothing magical about photosynthesis. It has however evolved over millions of years to the point where it can rather efficiently use solar energy to produce fuels. We believe that the production of an artificial leaf is possible and holds out the prospect of producing practical scalable systems for converting solar energy into fuel. Moreover, the need for such a system is so great that now is the time to invest in the research that is required to realize this dream. We see this as one of the grand challenges facing mankind and hope that enough of the really talented next generation of scientists will dedicate themselves to solving this challenge. Like all grand challenges it will not be easy but the result of not facing up to this challenge is impossible to contemplate.

Acknowledgements RJC acknowledges the support of the EPSRC. RJC and HH thank HFSP for support. HH and MN thank Nissan Science Foundation for support.

References

1. ESF report on "Harnessing solar energy for the production of clean fuels". http://ssnmr.leide-nuniv.nl/files/ssnmr/CleanSolarFuels.pdf

2. Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 428:287-292

3. Hofmann E, Wrench PM, Sharples FP, Hiller RG, Welte W, Diederichs K (1996) Structural basis of light harvesting by Carotenoids: peridinin-chlorophyll-protein from Amphidinium carterae. Science 272:1788-1791

4. McDermott G, Prince SM, Freer AA, Hawthornthwaite-Lawless AM, Papiz MZ, Cogdell RJ, Isaacs NW (1995) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374:517-521

5. Koepke J, Hu X, Muenke C, Schulten K, Michel H (1996) The crystal structure of the light-harvesting complex II (B800-850) from Rhodospirillum molischianum. Structure 4:581-597

6. Moser CC, Page CC, Cogdell RJ, Barber J, Wraight CA, Dutton PL (2003) Length, time, and energy scales of photosystems. Advances in protein chemistry. Academic, New York, pp. 71-109

7. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosyn-thetic oxygen-evolving center. Science 303:1831-1838

8. Sproviero EM, Gascon JA, McEvoy JP, Brudvig GW, Batista VS (2006) Characterization of synthetic oxomanganese complexes and the inorganic core of the O2-evolving complex in photosystem II: evaluation and the DFT/B3LYP level of theory. J Inorg Biochem 100:786-800

9. Vignais P, Billoud B (2007) Occurrence, classification, and biological function of hydroge-nases: an overview. Chem Rev 107:4206-4272

Getting Started With Solar

Getting Started With Solar

Do we really want the one thing that gives us its resources unconditionally to suffer even more than it is suffering now? Nature, is a part of our being from the earliest human days. We respect Nature and it gives us its bounty, but in the recent past greedy money hungry corporations have made us all so destructive, so wasteful.

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    How can we learn photosynthesis?
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