Energetics of Ionized Water Molecules in the H-Bond Network near the Ca2+ and Cl- Binding Sites in Photosystem II

Abstract

In photosystem II, water oxidation occurs at the oxygen-evolving complex (OEC). The presence of a hydronium ion (H₃O⁺) was proposed at the Cl^- binding site and Ca²⁺-depleted OEC. Using a quantum mechanical/molecular mechanical approach, we report the stability of H₃O⁺ in the PSII protein environment. Neither release of the proton from ligand water molecule W2 at the OEC nor formation of H₃O⁺ at Cl^- is energetically favorable. In contrast, H₃O⁺ can exist at the Ca²⁺-depleted OEC. Even when H₃O⁺ exists in Ca²⁺-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, E_m(TyrZ), remains unaltered. These observations explain why the oxidation of the Ca²⁺-depleted Mn₄O₅ cluster by TyrZ (i.e., the S₂ to S₃ transition) is not inhibited at low pH. It seems likely that Ca²⁺ plays a role in not only (i) maintaining the H-bond network and facilitating TyrZ oxidation [tuning E_m(TyrZ)] but also (ii) providing the valence of +2, decreasing the pK_a of the ligand molecule (W1), and facilitating the release of the proton from W1 in the S₂ to S₃ transition together with Cl^-.