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

Abstract

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 MnO 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 Mn₄ 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 MO 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 Mn₄ cluster and Y_Z. Connecting the observed reactivities of model complexes containing MO groups to spectroscopic information on the environment of the Mn₄ 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 MnO intermediate. In addition, a new role for Cl^– is proposed in which Cl^– tunes the nucleophilicity of the calcium-bound hydroxide.