A mechanistic and structural model for the formation and reactivity of a MnV=O species in photosynthetic water oxidation

Photosynthetic water oxidation is carried out by a tetranuclear Mn cluster contained in the membrane-bound protein complex photosystem II (PSII), The mechanism of PSII catalysed water oxidation is unknown; however, several current models invoke a high-valent Mn=O species as a key intermediate in O-O bond formation. In part, these proposals are based on biophysical studies of the protein which suggest that the redox-active tyrosine residue, Y-Z, abstracts hydrogen atoms directly from substrate water molecules bound to the Mn-4 cluster. In this paper, we consider organic oxidation and O-O bond-forming reactions catalysed by biomimetic Mn and Ru model complexes that are believed to proceed via M=O intermediates. We also interpret biophysical data concerning the roles of Ca2+ and Cl- in photosynthetic water oxidation, proposing that they are involved in a hydrogen-bonded network between the Mn-4 cluster and Y-Z. Connecting the observed reactivities of model complexes containing M=O groups to spectroscopic information on the environment of the Mn-4 cluster in the protein leads us to favour an O-O bond-forming step in photosynthetic water oxidation that occurs through nucleophilic attack. of a calcium-bound hydroxide ligand on the electrophilic oxygen atom of a Mn=O intermediate. In addition, a new role for Cl- is proposed in which Cl- tunes the nucleophilicity of the calcium-bound hydroxide.