Insights into the metalloradical mechanism of water oxidation

Abstract

Photosynthetic water oxidation occurs at an active site comprising four manganese atoms and an oxidizable tyrosine residue. Six years ago, at the Photosynthesis Congress at Montpellier, Jerry Babcock proposed a new mechanism by which that site might operate. In this metalloradical mechanism, the substrate water molecules bind to the manganese atoms as terminal ligands from which a tyrosine radical abstracts hydrogen atoms, thereby oxidizing the manganese cluster and advancing the ligands successively from aquo to hydroxo to oxo. Upon the fourth hydrogen atom abstraction, molecular oxygen is released. In the ensuing years, experimental work on inorganic model compounds and on Photosystem II itself has strongly supported the mechanism, while theoretical work has clarified the principles that govern the reaction. Recent work on cytochrome c oxidase indicates striking mechanistic similarities in its oxygen reduction reaction. Concerning Photosystem II, the hypothesis of electrically neutral oxidation of the manganese cluster enabled a shift in focus from manganese redox potentials to bond strengths of the ligands, especially the ligand O-H bonds. Thermodynamic cycles show that the ligand O-H bond strengths are determined by the strengths of the Mn-O bonds; these are determined by structural elements of the manganese complex. Knowledge of the bond strengths in the different S-states gives insight into the reactivity of the active site.