A mechanistic and structural model for the formation and reactivity of a MnV O 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, YZ, 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 YZ. 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.