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Photosynthetic Water Splitting Provides a Blueprint for Artificial Leaf Technology

2017; Elsevier BV; Volume: 1; Issue: 1 Linguagem: Inglês

10.1016/j.joule.2017.07.016

2542-4785

James Barber,

Advanced oxidation water treatment

He is a Fellow of the Royal Society (FRS), Fellow of the Royal Society of Chemistry (FRSC), Member of European Academy, and Foreign Member of the Swedish Royal Academy of Sciences. He has Honorary Doctorates of Stockholm University, University of East Anglia, and NTU. He has been awarded several medals and prizes including Flintoff Medal of RSC, Novartis Medal (UK Biochemical Society), Wheland Medal (University of Chicago), Eni-Ital gas/ENI Prize, Interdisciplinary Prize Medal of the RSC, Porter Medal of the International Photochemical Societies (Europe, USA, and Asia), and the Communication Award of the International Society of Photosynthesis Research. In 2009 he was the Lee Kuan Yew Distinguished Visitor to Singapore. Much of his research has focused on PSII and the water-splitting process that it catalyzes, and its crystal structure obtained in 2004. He is now investigating inorganic systems to mimic PSII in order to develop technology for non-polluting solar fuels. He is a Fellow of the Royal Society (FRS), Fellow of the Royal Society of Chemistry (FRSC), Member of European Academy, and Foreign Member of the Swedish Royal Academy of Sciences. He has Honorary Doctorates of Stockholm University, University of East Anglia, and NTU. He has been awarded several medals and prizes including Flintoff Medal of RSC, Novartis Medal (UK Biochemical Society), Wheland Medal (University of Chicago), Eni-Ital gas/ENI Prize, Interdisciplinary Prize Medal of the RSC, Porter Medal of the International Photochemical Societies (Europe, USA, and Asia), and the Communication Award of the International Society of Photosynthesis Research. In 2009 he was the Lee Kuan Yew Distinguished Visitor to Singapore. Much of his research has focused on PSII and the water-splitting process that it catalyzes, and its crystal structure obtained in 2004. He is now investigating inorganic systems to mimic PSII in order to develop technology for non-polluting solar fuels. The 2015 Paris Agreement on Climate Change (COP21), supported by 196 countries and so far ratified by 154 of them, specified a decarbonization of worldwide energy supply to minimize the average global temperature rise to less than 2°C of pre-industrial levels. This will require an 80% decrease in man-made CO2 emission by 2050 and to a zero level by the end of the century. Among renewable energy resources able to significantly tackle this challenge are nuclear fusion and solar. In both cases technological breakthroughs are required, with nuclear fusion proving to be very difficult. On the other hand, about one hour of sunlight falling on our planet is equivalent to all of the energy consumed by humans in an entire year, and we already have photovoltaic technology to capture it as electricity. However, if solar energy is to be a major primary energy source, it must be stored and dispatched on demand to the end user. An especially attractive approach is to store solar-converted energy in the form of chemical bonds as occurs in natural photosynthesis. However, a technology is needed that has a year-round average efficiency significantly higher than current plants or algae, to reduce land-area requirements and to be independent of food production. Therefore the scientific challenge is to construct an "artificial leaf" able to efficiently capture and convert solar energy and then store the energy in the form of chemical bonds, for example as hydrogen. The challenge to develop artificial photosynthesis as a major energy provider has to be undertaken against the backdrop of an ever increasing world population heading toward 10 billion by 2050. As a consequence it is likely that there will be a doubling of current energy consumption by 2050, of which at present over 80% is supplied by burning fossil fuels. In the case of natural photosynthesis, the initial energy-converting process is the light-driven splitting of water into its constituents parts (Equation 1).2H2O→4hvO2+4e−+4H+(Equation 1) In this way molecular oxygen is released to maintain our aerobic atmosphere while the "hydrogen" (electrons e− and proton H+) is used as the reducing power to convert carbon dioxide into the molecules that constitute life and the global biomass, as well as being the origin of our fossil fuels. The water-splitting enzyme of photosynthesis is called Photosystem II (PSII) and its evolution dates back at least 3 billion years.1Barber J. Photosystem II: the water splitting enzyme of photosynthesis and the origin of oxygen in our atmosphere.Q. Rev. Biophys. 2016; 49: 1-21Google Scholar The overall equation of photosynthesis (Equation 2) shows that for every molecule of O2 produced from two water molecules, one molecule of CO2 is converted into organic molecules such as carbohydrate (CH2O).2H2O+CO2→4hvO2+(CH2O)+H2O(Equation 2) Since today there is 21% O2 in the atmosphere, which as far as we know is derived entirely from photosynthesis, the amount of reduced carbon on our planet is enormous given that the atmospheric CO2 level is only 0.04%. This means that there is essentially an almost unlimited supply of fossil fuels, although presumably a great deal of the reduced carbon will not be readily obtainable. If it were, and if it was all burnt, our planet would return to its original anaerobic state with a very high level of CO2 in the atmosphere. I will touch on this issue again later in the article in relation to the development of artificial photosynthesis, but firstly I will summarize our current state of knowledge on how PSII catalyzes the light-driven splitting of water and the formation of the O-O bond. The importance of this fundamental chemical reaction, which is the entry point for the energy cycle of our planet, cannot be overstated. The water molecule is very stable and splitting it into its elemental constituents is thermodynamically and chemically demanding, especially when achieved in a delicate biological environment and powered by the relatively low energy content of four photons (4 hν) of long-wavelength visible light. Thus PSII provides a possible blueprint for the development of a scalable "artificial leaf" technology using solar radiation to extract hydrogen from water and provide a clean and renewable fuel.2Nocera D.G. The artificial leaf.Acc. Chem. Res. 2012; 45: 767-776Crossref PubMed Scopus (1360) Google Scholar The water-splitting reaction of PSII is a four-quantum process (Equation 1) involving five intermediate states (S0 to S4), whereby four oxidizing equivalents of about the same potential are sequentially accumulated at the catalytic site with absorption of each photon. The S4 state stores the four oxidizing equivalents needed to oxidize two water molecules to produce dioxygen (Equations 1 and 2) and in so doing reverts back to the S0 state. The oxidizing equivalents are stored by four Mn ions in the catalytic center, leading to four MnIV ions in the S3 state just before the last photochemical step to S4 (see Barber3Barber J. A mechanism for water splitting and oxygen production in photosynthesis.Nat. Plants. 2017; 3: 17041-17046Crossref PubMed Scopus (76) Google Scholar for references). The precise details of this final oxidation state are unknown because O-O bond formation is very fast. The cycle is powered by the oxidation of a chlorophyll known as P680 generated by light-driven primary charge separation in the reaction center of PSII coupled to a redox active tyrosine (YZ), serving as an intermediate electron carrier between P680+ and the Mn cluster.1Barber J. Photosystem II: the water splitting enzyme of photosynthesis and the origin of oxygen in our atmosphere.Q. Rev. Biophys. 2016; 49: 1-21Google Scholar With my colleagues at Imperial College London, we concluded from X-ray diffraction analysis of PSII crystals at 3.5-Å resolution that the oxygen-generating catalytic center of PSII consisted of a Mn3Ca2+O4 cubane with a fourth "dangler" Mn attached to the cubane via one of its bridging oxo bonds4Ferreira K.N. Iverson T.M. Maghlaoui K. Barber J. Iwata S. Architecture of the photosynthetic oxygen-evolving center.Science. 2004; 303: 1831-1838Crossref PubMed Scopus (2850) Google Scholar as shown in Figure 1A. Further refinement of this Mn4Ca2+O4 structure at 1.9 Å by Umena et al.5Umena Y. Kawakami K. Shen J.R. Kamiya N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å.Nature. 2011; 473: 55-60Crossref PubMed Scopus (3010) Google Scholar confirmed this geometry but added one additional bridging oxo between the external dangler Mn4 and the cubane to make an Mn4Ca2+O5 cluster (see Figure 1B). More recently an Mn4Ca2+O4 cluster has been synthesized in the absence of protein,6Zhang C. Chen C. Dong H. Shen J.R. Dau H. Zhao J. A synthetic Mn4Ca-cluster mimicking the oxygen-evolving center of photosynthesis.Science. 2015; 348: 690-693Crossref PubMed Scopus (371) Google Scholar and its structure is essentially identical to that proposed from my laboratory 11 years earlier (compare Figure 1A with 1C). Over the years there have been many postulates of the mechanism for O-O bond formation in PSII. Here I emphasize a chemical mechanism, the essence of which has been championed by several groups (see, for example, McEvoy and Brudvig8McEvoy J.P. Brudvig G.W. Water-splitting chemistry of photosystem II..Chem. Rev. 2006; 106: 4455-4483Crossref PubMed Scopus (1315) Google Scholar and Barber et al.9Barber J. Ferreira K. Maghlaoui K. Iwata S. Structural model of the oxygen-evolving centre of photosystem II with mechanistic implications.Phys. Chem. Chem. Phys. 2004; 6: 4737-4742Crossref Scopus (95) Google Scholar), which I favor and is consistent with the structure of the catalytic center of PSII.4Ferreira K.N. Iverson T.M. Maghlaoui K. Barber J. Iwata S. Architecture of the photosynthetic oxygen-evolving center.Science. 2004; 303: 1831-1838Crossref PubMed Scopus (2850) Google Scholar, 9Barber J. Ferreira K. Maghlaoui K. Iwata S. Structural model of the oxygen-evolving centre of photosystem II with mechanistic implications.Phys. Chem. Chem. Phys. 2004; 6: 4737-4742Crossref Scopus (95) Google Scholar As shown in Figure 2, the postulate is that dioxygen formation involves a substrate water, associated with the dangler Mn4, which is deprotonated during the S-state cycle and converted to a highly electrophilic oxo. This mechanism is dependent on Mn4 being converted to a high oxidation state (possibly MnV or a very reactive MnIV-oxyl radical) during progression to the S4 state just prior to O-O bond formation. The other three Mn ions are also in high valence state (3xMnIV) at this stage10Cox N. Retegan M. Neese F. Pantais D.A. Boussac A. Lubitz W. Electronic structure of the oxygen-evolving complex in photosystem II prior to O-O bond formation.Science. 2014; 345: 804-808Crossref PubMed Scopus (365) Google Scholar and act as a further "oxidizing battery" for the MnV-oxo or MnIV-oxyl radical species on Mn4. In this way the reactive oxo linked to Mn4 is electron deficient, so much so that it makes an ideal target for a nucleophilic attack by the oxygen of the second substrate water bound within the coordination sphere of the Ca2+. The deprotonation of the substrate waters would be aided by nearby basic amino acids while the weak Lewis acidity of Ca2+ allows the coordination of the substrate water to be ideally positioned for the nucleophilic attack. There is an extensive H-bonding network leading from the catalytic center to the outside of the PSII complex.5Umena Y. Kawakami K. Shen J.R. Kamiya N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å.Nature. 2011; 473: 55-60Crossref PubMed Scopus (3010) Google Scholar A very important aspect of this mechanism is that proton-coupled electron transfer occurs to avoid the buildup of a significant coulombic charge during the cycle, although one positive charge is accumulated during the S1 to S2 transition, which adds to the overall oxidizing potential of the Mn3Ca2+ cubane in the higher S states. To experimentally prove this mechanism, or any other alternative mechanism, will be a significant challenge. This is because the substrate for this enzyme is water and the reactants are H2O, OH, and O, which will require the application of techniques to detect changes at the level of individual protons. Nevertheless some very impressive X-ray free electron laser diffraction studies have recently been reported, but with resolutions not sufficiently good enough to detect protons and therefore identify a specific mechanism.11Young I.D. Ibrahim M. Chatterjee R. Gul S. Fuller F.D. Koroidov S. Brewster A.S. Tran R. Alonso-Mori R. Kroll T. Michels-Clark T. et al.Structure of photosystem II and substrate binding at room temperature.Nature. 2016; 540: 453-457Crossref PubMed Scopus (282) Google Scholar, 12Suga M. Akita F. Sugahara M. Kubo M. Nakajima Y. Nakane T. Yamashita K. Umena Y. Nakabayashi M. Yamane T. et al.Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL.Nature. 2017; 543: 131-135Crossref PubMed Scopus (428) Google Scholar For this reason, studies with synthetic model complexes play a role in this challenge. The hydroxyl/water nucleophilic attack concept for O-O bond formation has been demonstrated in Mn complexes with the involvement of MnV.13Gao Y. Åkermark T. Liu J. Sun L. Åkermark B. Nucleophilic attack of hydroxide on a MnV oxo complex: a model of the O-O bond formation in the oxygen evolving complex of photosystem II.J. Am. Chem. Soc. 2009; 131: 8726-8727Crossref PubMed Scopus (204) Google Scholar Moreover, the nucleophilic attack mechanism can be a dominant reaction for water splitting and oxygen formation by mononuclear Ru complexes oxidized by Ce4+ where the electrophile is Ru(V)=O and the nucleophile is solvent water.14Duan L. Wang L. Li F. Li F. Sun L. Highly efficient bioinspired molecular Ru water oxidation catalysts with negatively charged backbone ligands.Acc. Chem. Res. 2015; 48: 2084-2096Crossref PubMed Scopus (229) Google Scholar An interesting comparison between PSII and carbon monoxide dehydrogenase, which both extract "hydrogen" from water and have very similar geometries of their catalytic centers, also supports the nucleophilic mechanism on the surface of their Mn3Ca2+ and Fe3Ni2+ cubanes, respectively.3Barber J. A mechanism for water splitting and oxygen production in photosynthesis.Nat. Plants. 2017; 3: 17041-17046Crossref PubMed Scopus (76) Google Scholar The organo-metallo constructs, as well as PSII, tell us something about mechanisms for O-O bond formation but are unlikely to be incorporated into an "artificial leaf" technology because of fragility. What is needed are robust, non-toxic, and abundant water-splitting catalysts. They will also be required to use solar energy to power the reaction. The simplest design would be to use a semiconductor to absorb visible light and generate charge separation. Ideally the excited electrons in the conduction band should be sufficiently energetic to drive proton reduction to hydrogen while the holes left in the valence band have large enough oxidizing potentials to split water. In some cases the water-splitting process may occur at semiconductor surfaces but since the reaction is multi-electron, a bound catalyst may be required to achieve maximum rates. For this purpose, a wide range of metal oxides have been explored with Co oxide being particularly good,2Nocera D.G. The artificial leaf.Acc. Chem. Res. 2012; 45: 767-776Crossref PubMed Scopus (1360) Google Scholar while mixed metal oxides of iron and nickel are even better.15Hunter B.M. Blakemore J.D. Deimund M. Gray H.B. Winkler J.R. Müller A.M. Highly active mixed-metal nanosheet water oxidation catalysts made by pulsed-laser ablation in liquids.J. Am. Chem. Soc. 2014; 136: 13118-13121Crossref PubMed Scopus (250) Google Scholar, 16Hunter B.M. Gray H.B. Muller A.M. Earth-abundant heterogeneous water oxidation catalysts.Chem. Rev. 2016; 116: 14120-14136Crossref PubMed Scopus (1069) Google Scholar These co-catalysts have been employed with several semiconducting light-harvesting systems including triple-junction amorphous Si17Reece S.Y. Hamel J.A. Sung K. Jarvi T.D. Esswein A.J. Pijpers J.J. Nocera D.G. Wireless solar water splitting using silicon-based semiconductors and earth-abundant catalysts.Science. 2011; 334: 645-648Crossref PubMed Scopus (1376) Google Scholar and hematite (Fe2O3).18Gurudayal Sabba D. Kumar M.H. Wong L.H. Barber J. Grätzel M. Mathews N. Perovskite–hematite tandem cells for efficient overall solar driven water splitting.Nano Lett. 2015; 15: 3833-3839Crossref PubMed Scopus (214) Google Scholar Hematite is particularly attractive because it is cheap and non-toxic and a good absorber of the solar spectrum. Its band gap is 2.1 eV and the light-generated holes have sufficient oxidizing power (+2.0 eV) to split water. However, the conduction band potential is not low enough to produce hydrogen without some electrical bias. Similarly, PSII by itself cannot drive hydrogen production, and the bias is satisfied by a second light reaction taking place in photosystem I (PSI).1Barber J. Photosystem II: the water splitting enzyme of photosynthesis and the origin of oxygen in our atmosphere.Q. Rev. Biophys. 2016; 49: 1-21Google Scholar Hematite requires nanostructuring to reduce the extent of recombination reactions, and nanorods are proving to help overcome this problem. One artificial leaf device using them with Co as a co-catalyst has been assembled as shown in Figure 3.17Reece S.Y. Hamel J.A. Sung K. Jarvi T.D. Esswein A.J. Pijpers J.J. Nocera D.G. Wireless solar water splitting using silicon-based semiconductors and earth-abundant catalysts.Science. 2011; 334: 645-648Crossref PubMed Scopus (1376) Google Scholar Here the extra bias for hydrogen production is generated by the photovoltaic activity of a perovskite tightly coupled to the photoanode. This and other examples of photoelectrochemical systems17Reece S.Y. Hamel J.A. Sung K. Jarvi T.D. Esswein A.J. Pijpers J.J. Nocera D.G. Wireless solar water splitting using silicon-based semiconductors and earth-abundant catalysts.Science. 2011; 334: 645-648Crossref PubMed Scopus (1376) Google Scholar have only been explored at the laboratory level despite a worldwide explosion of research in this area. Given that at present the global power consumption is about 17.5 terawatts with the expectation of a significant increase by 2050 (see BP Energy Outlook, 2017 edition), artificial leaf technology is unlikely to have a significant impact on present and near-future energy supplies. However, it is always difficult to predict the emergence of new technology, and the present focus of attention on this area of solar energy capture and storage is vital and must continue to grow with urgency. It seems to me, given the demanding challenges of COP21, that more effort must now be directed at developing scalable technology, which must compete in financial terms with the relatively low cost and abundance of fossil fuels. For large-scale energy production the employment of photovoltaics to efficiently capture solar energy seems more realistic, subsequently using the photo-current at dedicated sites to drive water splitting using a new generation of efficient, low-cost electrochemical cells. Currently, electrolyzers for splitting water to obtain hydrogen on a large scale are too expensive. As mentioned above, low-cost non-toxic materials are being identified as alternatives to platinum for the electrochemical splitting of water. The establishment of a new generation of electrolyzers resulting from this research can also be used to store electricity derived from other sources such as wind and hydro, which are also solar driven, although they must have very good turnover rates to cope with the high level of energy delivery. The more tightly coupled systems, like that shown in Figure 3, may have application at the personal level such as individual houses and buildings, but will be especially important for remote areas where there is no grid and infrastructure, such as in underdeveloped countries.