Mechanistic and structural aspects of photosynthetic water oxidation

Conclusions on the functional and structural organisation of photosynthetic water oxidation are gathered from a critical survey of the wealth of data reported in the literature and author's own experimental research: (1) the water oxidising complex (WOC) contains a tetranuclear manganese cluster of 'dimer of dimers' structure and functional heterogeneity of the metal centers, (2) the four step univalent oxidative pathway leading to water oxidation into molecular oxygen and four protons comprises only manganese, tyrosine Y-Z of polypeptide D1 and the substrate as redox active species, (3) the redox transitions S-0 --> S-1 and S-1 --> S-2 are manganese centered whereas S-2 --> S-3 is most likely a ligand-centered reaction, (4) there exist several lines of evidence for a marked structural change that accompanies the redox transition S-2 --> S-3, (5) one Ca2+ is an indispensible constituent of a functionally competent WOC while the role of Cl- is much less clear and a direct participation disputable, (6) substrate water is most likely bound in all redox states S-0,...,S-3 and exchangeable with the bulk phase. The protonation state is determined by the redox state S-i and the protein microenvironment. A mechanism is proposed for water oxidation in the WOC that is based on three key postulates: (1) water oxidation takes place in the first coordination sphere of one manganese dimer [MnaMnb]; (2) the essential O-O bond is preformed in S-3 as part of a rapid redox isomerism S-3(I) <-> S-3(II) where in S-3(II) a nuclear geometry and electronic configuration is attained that corresponds to a peroxidic-type species; and (3) S-3(II) is an 'entatic state' for the formation of complexed dioxygen triggered by Y-Z(OX) induced electron abstraction from the WOC and electronic redistribution to S-0(O-2).