Reversible Structural Isomerization of Nature's Water Oxidation Catalyst Prior to O-O Bond Formation

Photosynthetic water oxidation is catalyzed by a manganese-calcium oxide cluster, which experiences five "S-states" during a light-driven reaction cycle. The unique "distorted chair"-like geometry of the Mn₄CaO₅₍₆₎ cluster shows structural flexibility that has been frequently proposed to involve "open" and "closed"-cubane forms from the S₁ to S₃ states. The isomers are interconvertible in the S₁ and S₂ states, while in the S₃ state, the open-cubane structure is observed to dominate inThermosynechococcus elongatus (cyanobacteria) samples. In this work, using density functional theory calculations, we go beyond the S₃⁺Y state to the S₃Y^• → S₄⁺Y step, and report for the first time that the reversible isomerism, which is suppressed in the S₃⁺Y state, is fully recovered in the ensuing S₃Y^• state due to the proton release from a manganese-bound water ligand. The altered coordination strength of the manganese-ligand facilitates formation of the closed-cubane form, in a dynamic equilibrium with the open-cubane form. This tautomerism immediately preceding dioxygen formation may constitute the rate limiting step for O₂ formation, and exert a significant influence on the water oxidation mechanism in photosystem II.