Release of a Proton and Formation of a Low-Barrier Hydrogen Bond between Tyrosine D and D2-His189 in Photosystem II

In photosystem II (PSII), the second-lowest oxidation state (S1) of the oxygen-evolving Mn4CaO5 cluster is the most stable, as the radical form of the redox-active D2-Tyr160 is considered to be a candidate that accepts an electron from the lowest oxidation state (S0) in the dark. Using quantum mechanical/molecular mechanical calculations, we investigated the redox potential (Em) of TyrD and its H-bond partner, D2-His189. The potential energy profile indicates that the release of a proton from the TyrD...D2-His189 pair leads to the formation of a low-barrier H-bond. The Em depends on the H+ position along the low-barrier H-bond, e.g., 680 mV when the H+ is at the D2-His189 moiety and 800 mV when the H+ is at the TyrD moiety, which can explain why TyrD mediates both the S0 to S1 oxidation and the S2 to S1 reduction.