Necessity of structural rearrangements for O-O bond formation between O5 and W2 in photosystem II

Abstract Numerous aspects of the water oxidation mechanism in photosystem II have not been fully elucidated, especially the O-O bond formation pathway. However, a body of experimental evidences have identified the O5 and W2 ligands of the oxygen-evolving complex as the highly probable substrate candidates. In this work, we studied O-O bond formation between O5 and W2 based on the native Mn4Ca cluster by density functional calculations. Structural rearrangements before the formation of the S4 state were found as a prerequisite for O-O bond formation between O5 and W2, regardless if the suggested pathways involving the typical Mn4(IV)-O• species or the recently proposed Mn4(VII)(O)2 species. Possible alternatives for the S2 → S3 and S3 → S4 transitions accounting for such required rearrangements are discussed. These findings reflect that the structural flexibility of the Mn4Ca cluster is essential to allow structural rearrangements during the catalytic cycle.