Spin, Valence, and Structural Isomerism in the S3 State of the Oxygen-Evolving Complex of Photosystem II as a Manifestation of Multimetallic Cooperativity

Photosynthetic water oxidation is catalyzed by a Mn4CaO5-cluster in photosystem II through an S-state cycle. Understanding the roles of heterogeneity in each S-state, as identified recently by the EPR spectroscopy, is very important to gain a complete description of the catalytic mechanism. We performed herein hybrid DFT calculations within the broken-symmetry formalism and associated analyses of Heisenberg spin models to study the electronic and spin structures of various isomeric structural motifs (hydroxo-oxo, oxyl-oxo, peroxo, and superoxo species) in the S(3 )state. Our extensive study reveals several factors that affect the spin ground state: (1) (formal) Mn oxidation state; (2) metal-ligand covalency; (3) coordination geometry; and (4) structural change of the Mn cluster induced by alternations in Mn...Mn distances. Some combination of these effects could selectively stabilize/destabilize some spin states. We found that the high spin state (S-total= 6) of the oxyl-oxo species can be causative for catalytic function, which manifests through mixing of the metal-ligand character in magnetic orbitals at relatively short 05...06 distances (<2.0 angstrom) and long Mn-A center dot center dot center dot O5 distances (>2.0 angstrom). These results will serve as a basis to conceptually identify and rationalize the physicochemical synergisms that can be evoked by the unique distorted chair topology of the cluster through cooperative Jahn-Teller effects on multimetallic centers.