Consequences of structural and biophysical studies for the molecular mechanism of photosynthetic oxygen evolution: functional roles for calcium and bicarbonate

Possible chemical mechanisms for catalyzing O-2 evolution from water in natural photosynthesis are summarized, based on the atomic and electronic structures of the inorganic core as revealed by spectroscopic and X-ray diffraction experiments and insights gained from inorganic complexes that achieve O-O bond formation. The thermodynamic and kinetic requirements for this multi-step reaction are reexamined, including the coupling of the individual electron-proton steps (PCET) and the O-O bond formation step. The four oxygen atoms at the corners of the proposed hetero-cubical Mn3CaO4 core (3 mu(3)-oxos and one mu(4)-oxo) can be distinguished by the number and types of chemical bonds to Ca2+ and Mn (geometries and orbital hybridization). Two of these mu(3)-oxos, postulated as substrates, are located at unique sites indicative of sp(2) + ppi hybridized orbitals. Both proposed substrate oxos are strongly hydrogen-bonded to different protein carboxylate residues, which are postulated as the initial proton transfer sites. Ca2+ is weakly bonded to these substrate oxos via non-directional ionic bonds that are postulated to provide stereochemical flexibility for the homolytic formation of the O-O bond. A previously postulated heterolytic pathway involving an electrophilic oxo and nucleophilic hydroxide species is reevaluated. We extend this mechanism by postulating roles for (bi)carbonate either in proton transfer or delivering the nucleophile for O-2 formation.