Energetics of Ionized Water Molecules in the H-Bond Network near the Ca and Cl Binding Sites in Photosystem II.

In photosystem II, water oxidation occurs at the oxygen-evolving complex (OEC). The presence of a hydronium ion (HO) was proposed at the Cl binding site and Ca-depleted OEC. Using a quantum mechanical/molecular mechanical approach, we report the stability of HO in the PSII protein environment. Neither release of the proton from ligand water molecule W2 at the OEC nor formation of HO at Cl is energetically favorable. In contrast, HO can exist at the Ca-depleted OEC. Even when HO exists in Ca-depleted PSII, the H-bond network of the redox-active tyrosine (TyrZ) remains unaltered, retaining the unusually short low-barrier H-bond with D1-His190, and the redox potential of TyrZ, (TyrZ), remains unaltered. These observations explain why the oxidation of the Ca-depleted MnO cluster by TyrZ (i.e., the S to S transition) is not inhibited at low pH. It seems likely that Ca plays a role in not only (i) maintaining the H-bond network and facilitating TyrZ oxidation [tuning (TyrZ)] but also (ii) providing the valence of +2, decreasing the p of the ligand molecule (W1), and facilitating the release of the proton from W1 in the S to S transition together with Cl.