Photobiological hydrogen production and artificial photosynthesis for clean energy: from bio to nanotechnologies

To convert the energy of sunlight into chemical energy, the leaf splits water via the photosynthetic process to produce molecular oxygen and hydrogen, which is in a form of separated protons and electrons. The primary steps of natural photosynthesis involve the absorption of sunlight and its conversion into spatially separated electron-hole pairs. The holes of this wireless current are captured by the oxygen evolving complex (OEC) of photosystem II (PSII) to oxidize water to oxygen. The electrons and protons produced as a byproduct of the OEC reaction are captured by ferrodoxin of photosystem I. With the aid of ferrodoxin-NADP(+) reductase, they are used to produce hydrogen in the form of NADPH. For a synthetic material to realize the solar energy conversion function of the leaf, the light-absorbing material must capture a solar photon to generate a wireless current that is harnessed by catalysts, which drive the four electron/hole fuel-forming water-splitting reaction under benign conditions and under 1 sun (100 mW/cm(2)) illumination. This Account describes the construction of an artificial leaf comprising earth-abundant elements by interfacing a triple junction, amorphous silicon photovoltaic with hydrogen- and oxygen-evolving catalysts made from a ternary alloy (NiMoZn) and a cobalt-phosphate cluster (Co-OEC), respectively. The latter captures the structural and functional attributes of the PSII-OEC. Similar to the PSII-OEC, the Co-OEC self-assembles upon oxidation of an earth-abundant metal ion from 2+ to 3+, may operate in natural water at room temperature, and is self-healing. The Co-OEC also activates H(2)O by a proton-coupled electron transfer mechanism in which the Co-OEC is increased by four hole equivalents akin to the S-state pumping of the Kok cycle of PSII. X-ray absorption spectroscopy studies have established that the Co-OEC is a structural relative of Mn(3)CaO(4)-Mn cubane of the PSII-OEC, where Co replaces Mn and the cubane is extended in a corner-sharing, head-to-tail dimer. The ability to perform the oxygen-evolving reaction in water at neutral or near-neutral conditions has several consequences for the construction of the artificial leaf. The NiMoZn alloy may be used in place of Pt to generate hydrogen. To stabilize silicon in water, its surface is coated with a conducting metal oxide onto which the Co-OEC may be deposited. The net result is that immersing a triple-junction Si wafer coated with NiMoZn and Co-OEC in water and holding it up to sunlight can effect direct solar energy conversion via water splitting. By constructing a simple, stand-alone device composed of earth-abundant materials, the artificial leaf provides a means for an inexpensive and highly distributed solar-to-fuels system that employs low-cost systems engineering and manufacturing. Through this type of system, solar energy can become a viable energy supply to those in the non-legacy world.

Because sunlight is diffuse and intermittent, substantial use of solar energy to meet humanity's needs will probably require energy storage in dense, transportable media via chemical bonds. Practical, cost effective technologies for conversion of sunlight directly into useful fuels do not currently exist, and will require new basic science. Photosynthesis provides a blueprint for solar energy storage in fuels. Indeed, all of the fossil-fuel-based energy consumed today derives from sunlight harvested by photosynthetic organisms. Artificial photosynthesis research applies the fundamental scientific principles of the natural process to the design of solar energy conversion systems. These constructs use different materials, and researchers tune them to produce energy efficiently and in forms useful to humans. Fuel production via natural or artificial photosynthesis requires three main components. First, antenna/reaction center complexes absorb sunlight and convert the excitation energy to electrochemical energy (redox equivalents). Then, a water oxidation complex uses this redox potential to catalyze conversion of water to hydrogen ions, electrons stored as reducing equivalents, and oxygen. A second catalytic system uses the reducing equivalents to make fuels such as carbohydrates, lipids, or hydrogen gas. In this Account, we review a few general approaches to artificial photosynthetic fuel production that may be useful for eventually overcoming the energy problem. A variety of research groups have prepared artificial reaction center molecules. These systems contain a chromophore, such as a porphyrin, covalently linked to one or more electron acceptors, such as fullerenes or quinones, and secondary electron donors. Following the excitation of the chromophore, photoinduced electron transfer generates a primary charge-separated state. Electron transfer chains spatially separate the redox equivalents and reduce electronic coupling, slowing recombination of the charge-separated state to the point that catalysts can use the stored energy for fuel production. Antenna systems, employing a variety of chromophores that absorb light throughout the visible spectrum, have been coupled to artificial reaction centers and have incorporated control and photoprotective processes borrowed from photosynthesis. Thus far, researchers have not discovered practical solar-driven catalysts for water oxidation and fuel production that are robust and use earth-abundant elements, but they have developed artificial systems that use sunlight to produce fuel in the laboratory. For example, artificial reaction centers, where electrons are injected from a dye molecule into the conduction band of nanoparticulate titanium dioxide on a transparent electrode, coupled to catalysts, such as platinum or hydrogenase enzymes, can produce hydrogen gas. Oxidizing equivalents from such reaction centers can be coupled to iridium oxide nanoparticles, which can oxidize water. This system uses sunlight to split water to oxygen and hydrogen fuel, but efficiencies are low and an external electrical potential is required. Although attempts at artificial photosynthesis fall short of the efficiencies necessary for practical application, they illustrate that solar fuel production inspired by natural photosynthesis is achievable in the laboratory. More research will be needed to identify the most promising artificial photosynthetic systems and realize their potential.

Photosynthesis converts light energy into biologically useful chemical energy vital to life on Earth. The initial reaction of photosynthesis takes place in photosystem II (PSII), a 700-kilodalton homodimeric membrane protein complex that catalyses photo-oxidation of water into dioxygen through an S-state cycle of the oxygen evolving complex (OEC). The structure of PSII has been solved by X-ray diffraction (XRD) at 1.9 ångström resolution, which revealed that the OEC is a Mn4CaO5-cluster coordinated by a well defined protein environment. However, extended X-ray absorption fine structure (EXAFS) studies showed that the manganese cations in the OEC are easily reduced by X-ray irradiation, and slight differences were found in the Mn-Mn distances determined by XRD, EXAFS and theoretical studies. Here we report a 'radiation-damage-free' structure of PSII from Thermosynechococcus vulcanus in the S1 state at a resolution of 1.95 ångströms using femtosecond X-ray pulses of the SPring-8 ångström compact free-electron laser (SACLA) and hundreds of large, highly isomorphous PSII crystals. Compared with the structure from XRD, the OEC in the X-ray free electron laser structure has Mn-Mn distances that are shorter by 0.1-0.2 ångströms. The valences of each manganese atom were tentatively assigned as Mn1D(III), Mn2C(IV), Mn3B(IV) and Mn4A(III), based on the average Mn-ligand distances and analysis of the Jahn-Teller axis on Mn(III). One of the oxo-bridged oxygens, O5, has significantly longer distances to Mn than do the other oxo-oxygen atoms, suggesting that O5 is a hydroxide ion instead of a normal oxygen dianion and therefore may serve as one of the substrate oxygen atoms. These findings provide a structural basis for the mechanism of oxygen evolution, and we expect that this structure will provide a blueprint for the design of artificial catalysts for water oxidation.