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Abstract

The Mn₄CaO₅₍₆₎ cluster in photosystem II catalyzes water splitting through the S_i state cycle (i = 0–4). Molecular O₂ is formed and the natural catalyst is reset during the final S₃ → (S₄) → S₀ transition. Only recently experimental breakthroughs have emerged for this transition but without explicit information on the S₀-state reconstitution, thus the progression after O₂ release remains elusive. In this report, our molecular dynamics simulations combined with density functional calculations suggest a likely missing link for closing the cycle, i.e., restoring the first catalytic state. Specifically, the formation of closed-cubane intermediates with all hexa-coordinate Mn is observed, which would undergo proton release, water dissociation, and ligand transfer to produce the open-cubane structure of the S₀ state. Thereby, we theoretically identify the previously unknown structural isomerism in the S₀ state that acts as the origin of the proposed structural flexibility prevailing in the cycle, which may be functionally important for nature’s water oxidation catalysis.