Abstract
The Mn(4)CaO(5(6)) cluster in photosystem II catalyzes water splitting through the S(i) state cycle (i = 0-4). Molecular O(2) is formed and the natural catalyst is reset during the final S(3) → (S(4)) → S(0) transition. Only recently experimental breakthroughs have emerged for this transition but without explicit information on the S(0)-state reconstitution, thus the progression after O(2) 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 S(0) state. Thereby, we theoretically identify the previously unknown structural isomerism in the S(0) 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.