The interaction of His337 with the Mn4Ca cluster of photosystem II

The most recent XRD studies of Photosystem II (PS II) reveal that the His337 residue is sufficiently close to the Mn(4)Ca core of the Water Oxidising Complex (WOC) to engage in H-bonding interactions with the μ(3)-oxo bridge connecting Mn(1), Mn(2) and Mn(3). Such interactions may account for the lengthening of the Mn-Mn distances observed in the most recent and highest resolution (1.9 ?) crystal structure of PS II compared to earlier, lower-resolution (2.9 ? or greater) XRD structures and EXAFS studies on functional PS II. Density functional theory is used to examine the influence on Mn-Mn distances of H-bonding interactions, mediated by the proximate His337 residue, which may lead to either partial or complete protonation of the μ(3)-oxo bridge on models of the WOC. Calculations were performed on a set of minimal-complexity models (in which WOC-ligating amino acid residues are represented as formate and imidazole ligands), and also on extended models in which a 13-peptide sequence (from His332 to Ala344) is treated explicitly. These calculations demonstrate that while the 2.9 ? structure is best described by models in which the μ(3)-oxo bridge is neither protonated nor involved in significant H-bonding, the 1.9 ? XRD structure is better reproduced by models in which the μ(3)-oxo bridge undergoes H-bonding interactions with the His337 residue leading to expansion of the 'close' Mn-Mn distances well known from EXAFS studies at ～ 2.7 ?. Furthermore, full μ(3)-oxo-bridge protonation remains a distinct possibility during the process of water oxidation, as evidenced by the lengthening of the Mn-Mn vectors observed in EXAFS studies of the higher oxidation states of PS II. In this context, the Mn-Mn distances calculated in the protonated μ(3)-oxo bridge structures, particularly for the peptide extended models, are in close agreement with the EXAFS data.