The interaction of His337 with the Mn ₄Ca 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 ₄Ca 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 Å) crystal structure of PS II compared to earlier, lower-resolution (2.9 Å 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 Å 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 Å 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 Å. 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.