The manganese complex of photosystem II in its reaction cycle—Basic framework and possible realization at the atomic level

Photosynthetic water oxidation proceeds at a pentanuclear Mn4Ca complex bound to amino acid residues in the interior of photosystem II (PSII). It involves the binding of two water molecules, the removal of four electrons and four protons from the Mn-complex/substrate-water entity, O–O bond formation, and dioxygen release. Basic aspects of the reaction cycle of the Mn complex of PSII are discussed: (1) Kok's classical S-state cycle and the corresponding experimental paradigm; (2) recent observations on the (still) enigmatic S4 state; (3) sequence and characteristics of electron transfer and proton release; (4) a basic nine-step reaction cycle involving eight steps of alternating deprotonation and oxidation of the Mn-complex prior to O–O bond formation and dioxygen release; (5) the energetic constraints of water oxidation in PSII and their mechanistic consequences. In the second part it is considered how the suggested nine-step reaction cycle possibly is realized at the atomic level: (i) studies on synthetic Mn complexes suggest that deprotonation of μ-hydroxo bridges or formation of new μ-oxo bridges could facilitate successive oxidation steps without prohibitive potential increase. (ii) Current structural models of the PSII Mn complex derived from X-ray absorption spectroscopy and/or protein crystallography are discussed. (iii) Structural and oxidation-state changes of the Mn complex are related to the basic nine-step reaction cycle. (iv) As a framework for mechanistic models at the atomic level, we propose that water is oxidized only after the accumulation of four bases which function as proton acceptors in the dioxygen formation step.