Spin, Valence, and Structural Isomerism in the S 3 State of the Oxygen-Evolving Complex of Photosystem II as a Manifestation of Multimetallic Cooperativity

Hiroshi Isobe, Mitsuo Shoji, Takayoshi Suzuki, Jian Ren Shen, Kizashi Yamaguchi

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    13 Citations (Scopus)


    Photosynthetic water oxidation is catalyzed by a Mn 4 CaO 5 -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 O5···O6 distances (<2.0 Å) and long Mn A ···O5 distances (>2.0 Å). 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.

    Original languageEnglish
    Pages (from-to)2375-2391
    Number of pages17
    JournalJournal of Chemical Theory and Computation
    Issue number4
    Publication statusPublished - Apr 9 2019

    ASJC Scopus subject areas

    • Computer Science Applications
    • Physical and Theoretical Chemistry


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