Abstract
The mechanism of water oxidation catalyzed by Mn(4)CaO(5) in photosystem II lacks consensus, particularly regarding proton-coupled electron transfer in the second flash-induced S(2) to S(3) transition. Here, we investigate the electron transfer mechanism during the S(2) to S(3) 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 Ca(2+) (W3), but from a ligand water molecule (W1) near D1-Asp61 at Mn4, forming OH(-) at Mn-(IV). OH(-) formation at Ca(2+) is significantly less stable than that at Mn4-(IV). Incorporation of the OH(-) species into Mn(4)CaO(5) 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 S(2) to S(3) transition, significantly smaller than those between Mn4 and TyrZ in the S(0) to S(1) (∼170 meV) and S(1) to S(2) (∼120 meV) transitions. This step serves as the rate-limiting step if [Mn-(IV)](4) is considered to be the relevant state to S(3).