Substitution of Ca²⁺ and changes in the H-bond network near the oxygen-evolving complex of photosystem II

Ca²⁺, which provides binding sites for ligand water molecules W3 and W4 in the Mn₄CaO₅ cluster, is a prerequisite for O₂ evolution in photosystem II (PSII). We report structural changes in the H-bond network and the catalytic cluster itself upon the replacement of Ca²⁺ with other alkaline earth metals, using a quantum mechanical/molecular mechanical approach. The small radius of Mg²⁺ makes W3 donate an H-bond to D1-Glu189 in Mg²⁺-PSII. If an additional water molecule binds at the large surface of Ba²⁺, it donates H-bonds to D1-Glu189 and the ligand water molecule at the dangling Mn, altering the H-bond network. The potential energy profiles of the H-bond between D1-Tyr161 (TyrZ) and D1-His190 and the interconversion between the open- and closed-cubane S₂ conformations remain substantially unaltered upon the replacement of Ca²⁺. Remarkably, the O5⋯Ca²⁺ distance is shortest among all O5⋯metal distances irrespective of the radius being larger than that of Mg²⁺. Furthermore, Ca²⁺ is the only alkaline earth metal that equalizes the O5⋯metal and O2⋯metal distances and facilitates the formation of the symmetric cubane structure.