Structural Studies of Oxomanganese Complexes for Water Oxidation Catalysis

Photosynthetic water-splitting into O2, protons and electrons is a thermodynamically demanding 4-electron oxidation reaction catalyzed by the oxygen-evolving complex (OEC) of photosystem II (PSII). Recent breakthroughs in X-ray crystallography have resolved the structure of PSII at 1.9 Å resolution, providing fundamental insights on the structure of the OEC, including characterization of the oxomanganese cluster and its ligation scheme by water and proteinaceous side chains. However, simulations of high-resolution extended X-ray absorption fine structure (EXAFS) spectra based on the X-ray model and direct comparisons with EXAFS measurements have suggested reductive damage caused by the high doses of X-ray radiation. Therefore, density functional theory (DFT) and quantum mechanics/molecular mechanics (QM/MM) hybrid methods have been combined to obtain a model OEC in the dark-adapted state most consistent with both high resolution spectroscopy and X-ray diffraction data. DFT studies of biomimetic oxomanganese complexes, including the analysis of O2 evolution catalyzed by the Mn terpy dimer [H2O(terpy)MnIII(μ-O)2MnIV(terpy)OH2]3+ (1, terpy=2,2′:6′,2″-terpyridine), have provided valuable insights on fundamental aspects of the water splitting mechanism. These computational studies suggest that acid/base cofactors present in the buffer environment surrounding the oxomanganese core play a crucial role in the kinetics of O-O bond formation. Similar regulation of catalytic activity is expected to be induced by acid/base cofactors in PSII surrounding the OEC, or by the electrolyte buffer in artificial photosynthetic devices based on biomimetic oxomanganese complexes bound to semiconductor surfaces.