No abstract

In this article, we give an overview of nature's singular biological process for producing oxygen gas by the oxidation of water in photosynthetic organisms. The harnessing of light to accomplish the splitting of water was arguably nature's most successful experiment in biological innovation. It enabled global proliferation of oxygenic photosynthesis and created the biogeochemical cycles of oxygen and carbon on earth. We review the atomic structure of the metalloenzyme, the photosystem II water splitting complex (PSII‐WOC), as revealed by X‐ray diffraction and spectroscopic techniques. We describe: 1) The electronic structure of its inorganic core, Mn 4 Ca 1 O x Cl 1–2 (HCO 3 ) y , based upon spectroscopic and magnetic susceptibility measurements, 2) the organization of the protein subunits as revealed by X‐ray diffraction and the role of select amino acid residues as revealed by site‐directed mutagenesis, and 3) the kinetic sequence of steps during assembly of the inorganic core to the cofactor‐depleted apo‐protein and the functional consequences of substitution of the inorganic cofactors. We use these data together with physico‐chemical data describing the formation of light‐induced intermediates, the exchange rates between substrate and free water molecules, the stoichiometry of electron and proton release and the activation energies to discuss possible mechanisms for photosynthetic water splitting. The chemistry of photosynthetic water splitting is energetically demanding and mechanistically complex. The lessons learned from nature have guided chemists seeking to incorporate these design principles within catalysts suitable for abiotic water splitting. We end with a description of the few synthetic manganese complexes that have been found to produce oxygen gas from water and discuss the chemical mechanisms by which they appear to function.

In this article, we give an overview of nature's singular biological process for producing oxygen gas by the oxidation of water in photosynthetic organisms. The harnessing of light to accomplish the splitting of water was arguably nature's most successful experiment in biological innovation. It enabled global proliferation of oxygenic photosynthesis and created the biogeochemical cycles of oxygen and carbon on earth. We review the atomic structure of the metalloenzyme, the photosystem II water splitting complex (PSII‐WOC), as revealed by X‐ray diffraction and spectroscopic techniques. We describe: 1) The electronic structure of its inorganic core, Mn 4 Ca 1 O x Cl 1–2 (HCO 3 ) y , based upon spectroscopic and magnetic susceptibility measurements, 2) the organization of the protein subunits as revealed by X‐ray diffraction and the role of select amino acid residues as revealed by site‐directed mutagenesis, and 3) the kinetic sequence of steps during assembly of the inorganic core to the cofactor‐depleted apo‐protein and the functional consequences of substitution of the inorganic cofactors. We use these data together with physico‐chemical data describing the formation of light‐induced intermediates, the exchange rates between substrate and free water molecules, the stoichiometry of electron and proton release and the activation energies to discuss possible mechanisms for photosynthetic water splitting. The chemistry of photosynthetic water splitting is energetically demanding and mechanistically complex. The lessons learned from nature have guided chemists seeking to incorporate these design principles within catalysts suitable for abiotic water splitting. We end with a description of the few synthetic manganese complexes that have been found to produce oxygen gas from water and discuss the chemical mechanisms by which they appear to function.