Electron Transfer Mechanism from the Oxygen-Evolving Complex to the Electron-Acceptor Tyrosine during the S₂ to S₃...

The mechanism of water oxidation catalyzed by Mn₄CaO₅ in photosystem II lacks consensus, particularly regarding proton-coupled electron transfer in the second flash-induced S₂ to S₃ transition. Here, we investigate the electron transfer mechanism during the S₂ to S₃ transition using a quantum mechanical/molecular mechanical/polarizable continuum model approach. The electrostatic interaction with the oxidized redox-active tyrosine, TyrZ, triggers proton release not from a ligand water molecule near chloride (W2) at dangling Mn (Mn4) or a ligand water molecule at Ca²⁺ (W3), but from a ligand water molecule (W1) near D1-Asp61 at Mn4, forming OH^- at Mn-(IV). OH^- formation at Ca²⁺ is significantly less stable than that at Mn4-(IV). Incorporation of the OH^- species into Mn₄CaO₅ induces a valence-state conversion from (III,IV,IV,IV) to (IV,IV,IV,III). Interestingly, subsequent water incorporation from a water channel and restoration of the H-bond network of TyrZ not only elevate the redox potential of TyrZ but also convert the valence state back to (III,IV,IV,IV), facilitating electron transfer to TyrZ. The electronic coupling between Mn1 and TyrZ is 1 to 3 meV in the S₂ to S₃ transition, significantly smaller than those between Mn4 and TyrZ in the S₀ to S₁ (∼170 meV) and S₁ to S₂ (∼120 meV) transitions. This step serves as the rate-limiting step if [Mn-(IV)]₄ is considered to be the relevant state to S₃.