Toward the assignment of the manganese oxidation pattern in the water-oxidizing complex of photosystem II: a time-dependent DFT study of XANES energies.

Density functional theory (DFT) and time-dependent DFT (TDDFT) calculations are reported on three sets of isomeric models of the {Mn(4)/Ca} water-oxidizing complex of photosystem II (PS II), which share the general formula [CaMn(4)O(4)(N(2)C(3)H(4))(RCOO)(6)](q)⋅(H(2)O)(n) (R=H, CH(3); q=-1, 0, +1, +2; n=3, 4, 5, 6, 7). Comparison with the full range of available data on Mn K-edge X-ray absorption energy values determined for the photosystem allows us to validate the structures that correspond to the particular S states and to determine their Mn oxidation patterns. By using a new TDDFT procedure, it is shown that variations in the absolute K-edge energy values for a particular S state, reported by different research groups, can be quantitatively explained by different geometries adopted by the Mn cluster, which demonstrates flexibility in the position of the fourth 'dangling' Mn atom in relation to a cubane structure created by the Ca atom and the three other Mn atoms. Computational results show that each step of the S cycle occurs by removal of one electron directly from the Mn cluster. This Mn-centered oxidation still agrees with the small difference observed experimentally between the K-edge energy values of the S(2) and S(3) states of the photosystem, thus resolving a controversy as to whether this represents ligand-centered or metal-centered oxidation. The overall oxidation state of Mn atoms in the tetramanganese cluster during functional turnover changes from 2.75 for S(0), 3.00 for S(1), and 3.25 for S(2) up to 3.50 for the S(3) state, which is systematically 0.50 lower than the previously proposed oxidation states of the cluster. The calculations give insight into why these earlier, purely empirical, assignments of the Mn oxidation levels in PS II could be in error.