A Low‐Oxidation‐State Mechanism for O─O Bond Formation in Photosystem II via Oxo–Hydroxyl Radical Coupling

ABSTRACT In this computational work, we identify an oxo–hydroxyl radical coupling (OHC) mechanism for O─O bond formation in PSII within the low‐oxidation‐state (LOS) paradigm, in which the Ca‐bound W 3 water and O5 act as the substrates. While several recent crystallographic and computational studies indicate that the O x ligand is absent in the S 3 state, we show that it forms upon entry into the S 4 state through migration of the Ca‐bound water ligand W 3 into the cavity between Mn1 and Ca 2 + . From this intermediate, O x ─O5 bond formation proceeds via the OHC mechanism rather than the conventional oxo–oxyl pathway. This mechanism leads to formation of a hydroperoxide intermediate as the lowest‐energy post‐coupling species, in which Mn1 is reduced to the III oxidation state. Jahn–Teller distortion considerably weakens the Mn1(III)─O x bond, explaining the poor resolution of O x in XFEL structures following O─O bond formation, an observation difficult to reconcile within conventional high‐oxidation‐state (HOS) models. Importantly, the proposed mechanism is consistent with water‐exchange experiments identifying W 3 and O5 as the substrate oxygen atoms. The mechanistic insights obtained in this work enabled us to propose likely S state structures and proton‐release assignments within the Kok cycle.