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

Abstract

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 Tyrzox 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.