Structure and reactivity of the mixed-valence CaMn₄O ₅(H₂O)₄ and CaMn₄O ₄(OH)(H₂O)₄ clusters at oxygen evolution complex of photosystem II. Hybrid DFT (UB3LYP and UBHandHLYP) calculations

Very recently Umena et al. have determined the X-ray diffraction (XRD) structure of the CaMn₄O₅ cluster in the oxygen evolution complex (OEC) of photosystem II (PSII) refined to 1.9 Å resolution. We have performed theoretical attempts to elucidate possible electronic and spin states of their new XRD structure of the CaMn₄O₅ cluster. For the purpose, hybrid density functional theory (UB3LYP and UBHandHLYP) calculations have been performed for the mixed-valence (MV) CaMn(III) _4-ω(IV)_ωO₅(H₂O) ₄ (1) and CaMn(III)_4-ω(IV)_ωO ₄(OH)(H₂O)₄ (2) clusters as active catalytic site for water splitting reaction in OEC of PSII. Full geometry optimizations of 1a (ω = 2) and 2a (ω = 2) have been performed to elucidate scope and limitation of the cluster models. Both charge and spin fluctuated structures (48 UB3LYP solutions) have been considered for the MV 1a (ω = 2). Total energies obtained by these calculations have elucidated quasi-degenerated electronic and spin states that are characterized by charge and spin density populations. The energy levels revealed by hybrid DFT are analyzed on the basis of the Heisenberg spin Hamiltonian model, providing the effective exchange integrals between manganese ions at a uniform or MV structure. The spin projections for hybrid DFT solutions are performed using the effective exchange integrals. The charge fluctuation model is introduced to analyze relative stabilities among MV structures of 1a and 2a. These computational results for 1a and 2a have explored several characteristic electronic properties of the species that are used for theoretical elucidation of possible mechanisms of water splitting reaction. Orbital and spin correlation diagrams are derived for the O-O bond formation and oxygen evolution in the reaction. Implications of the computational results are also discussed in relation to available experiments and theoretical results by other groups.