Model of the Oxygen Evolving Complex Which Is Highly Predisposed to O-O Bond Formation

Light-driven water oxidation is a fundamental reaction in the biosphere. The Mn₄Ca cluster of photosystem II cycles through five redox states termed S₀-S₄, after which oxygen is evolved. Critically, the timing of O-O bond formation within the Kok cycle remains unknown. By combining recent crystallographic, spectroscopic, and DFT results, we demonstrate an atomistic S₃ state model with the possibility of a low barrier to O-O bond formation prior to the final oxidation step. Furthermore, the associated one electron oxidized S₄ state does not provide more advantages in terms of spin alignment or the energy of O-O bond formation. We propose that a high energy peroxide isoform of the S₃ state can preferentially be oxidized by Tyr _z^ox in the course of final electron transfer leading to O₂ evolution. Such a mechanism may explain the peculiar kinetic behavior of O₂ evolution as well as serve as an evolutionary adaptation to avoid release of the harmful peroxides.