Structural, magnetic coupling and oxidation state trends in models of the CaMn₄ cluster in photosystem II

Density functional theory calculations are reported on a set of isomeric structures I, II and III that share the structural formula [CaMn ₄C₉H₁₀N₂O₁₆] ^q+·(H₂O)₃ (q = -l, 0, 1, 2, 3). Species I has a skeletal structure, which has been previously identified as a close match to the ligated CaMn4 cluster in Photosystem II, as characterized in the most recent 3.0 Å crystal structure. Structures II and III are rearrangements of I, which largely retain that model's bridging ligand framework, but feature metal atom positions broadly consistent with, respectively, the earlier 3.5 and 3.2 Å crystal structures for the Photosystem II water-oxidising complex (WOC). Our study explores the influence of the cluster charge state (and hence S state) on several important properties of the model structures; including the relative energies of the three models, their interconversion, trends in the individual Mn oxidation states, preferred hydration sites and favoured modes of magnetic coupling between the manganese atoms. We find that, for several of the explored cluster charge states, modest differences in the bridging-ligand geometry exert a powerful influence over the individual manganese oxidation states, but throughout these states the robustness of the tetrahedron formed by the Ca and three of the Mn atoms remains a significant feature and contrasts with the positional flexibility of the fourth Mn atom. Although structure I is lowest in energy for most S states, the energy differences between structures for a given S state are not large. Overall, structure II provides a better match for the EXAFS derived metal-metal distance parameters for the earlier S states (S₀ to S₂), but not for S₃ in which a significant structural change is observed experimentally. In this S state structure III provides a closer fit. The implications of these results, for the possible action of the WOC, are discussed.