Theory of chemical bonds in metalloenzymes XIX: Labile manganese oxygen bonds of the CaMn₄O₅ cluster in oxygen evolving complex of photosystem II

Spin polarisation effects of labile manganese-oxygen bonds in the X-ray diffraction structure of the oxygen-evolving complex (OEC) of photosystem II (PSII) at 1.9 Å resolution have been investigated by the UB3LYP computations on the basis of three different theoretical models with and without hydrogen bonds: quantum-mechanical (QM) Model I, QM(Model II)/MM and QM Model III. The spin densities on the manganese and oxygen atoms of the CaMn ₄O₅ cluster revealed by these computations have elucidated internal, semi-internal and external reductions of high-valent manganese ions in the CaMn₄O₅ cluster in OEC of PSII. The internal reduction of Mn(IV) ions by the back charge transfer from oxygen dianions is remarkable in the small QM Model I, whereas it is significantly reduced in the case of more realistic QM Model III including hydrogen bonding stabilisations of oxygen dianions. However, semi-internal reduction of the CaMn₄O ₅ cluster with remote amino acid residues such as Asp61 anion occurs even in QM Model III, indicating the necessity of large QM parts for redox-active systems such as OEC of PSII. The computational results have clearly demonstrated important roles of confinement effects of the CaMn ₄O₅ cluster with labile Mn-O bonds with protein. These computational results have been applied to molecular design of artificial robust catalysts for water oxidation by use of sunlight.