Manganese oxyl radical intermediates and O-O bond formation in photosynthetic oxygen evolution and a proposed role for the calcium cofactor in photosystem II

Spin state considerations are proposed to sharply limit the possible O-O bond-forming steps in water oxidation by the oxygen evolving center of Photosystem II. A series of intermediates are proposed for the Kok S states on the basis of quantum chemical studies on simple model complexes; these are also consistent with the main biophysical data. Only one Mn atom in the active site cluster is thought to be redox-active and mediate O-O bond formation. A key concept is the formation of an unreactive Mn=O oxo at the S(2) state, followed by its conversion to a reactive Mn-O . oxyl form at the S(3) level, with radical character on the oxyl oxygen, at which point O-O bond formation can occur by a coupling between the oxyl and an outer-sphere water molecule. An MnOOH intermediate at S(3) is proposed to lose a hydrogen atom to give O(2). The role of the Ca cofactor is to bring about a 5- to 6-coordination change at S(2), necessary for formation of a reactive oxo in S(3). The chloride cofactor is assigned the role of charge neutralization.