A Hydroxyl Radical Model for the S3 State of Photosystem II

Abstract The chemical identity of the oxygen-evolving complex (OEC) in the metastable heterogeneous S3 state that precedes water oxidation remains intensely debated. Multiple ideas regarding the oxidation states of the four constituent Mn ions, as well as the number and protonation states of oxygen ligands are being considered, entailing distinct mechanistic pathways for the subsequent O–O bond formation. Here we describe a previously unreported possibility for the OEC in the S3 state identified by quantum chemical calculations. The model contains a hydroxyl radical that is bridging a terminal Mn center and the redox-inactive Ca2+ ion. In contrast to past ligand-radical suggestions the hydroxyl radical form has a crystallographically consistent intracluster O···O distance of 2.0 Å, while its total proton count is fully aligned with experimental data. Calculations suggest that the hydroxyl radical intermediate has a low-spin or diamagnetic ground state. Importantly, its unusual excited state profile make it a rare, though not definitive, candidate for the near-infrared absorbing component of the S3 state. The hydroxyl radical model enriches our perspectives on S3 state heterogeneity and expands the map of structure–property correlations in biological water oxidation.