Theory of chemical bonds in metalloenzymes XXII: a concerted bond-switching mechanism for the oxygen-oxygen bond formation coupled with one electron transfer for water oxidation in the oxygen-evolving complex of photosystem II

摘要

QM(UB3LYP)/MM(AMBER) calculations were performed for the locations of the transition structure (TS) of the oxygen-oxygen (O-O) bond formation in the S-4 state of the oxygen-evolving complex (OEC) of photosystem II (PSII). The natural orbital (NO) analysis of the broken-symmetry (BS) solutions was also performed to elucidate the nature of the chemical bonds at TS on the basis of several chemical indices defined by the occupation numbers of NO. The computational results revealed a concerted bond switching (CBS) mechanism for the oxygen-oxygen bond formation coupled with the one-electron transfer (OET) for water oxidation in OEC of PSII. The orbital interaction between the sigma-HOMO of the Mn(IV)(4)-O-(5) bond and the pi*-LUMO of the Mn(V)(1)=O-(6) bond plays an important role for the concerted O-O bond formation for water oxidation in the CaMn4O6 cluster of OEC of PSII. One electron transfer (OET) from the pi-HOMO of the Mn(V)(1)=O-(6) bond to the sigma*-LUMO of the Mn(IV)(4)-O-(5) bond occurs for the formation of electron transfer diradical, where the generated anion radical [Mn(IV)(4)-O-(5)](-)center dot part is relaxed to the center dot Mn(III)(4) horizontal ellipsis O-(5)(-) structure and the cation radical [O-(6)=Mn(V)(1)](+) center dot part is relaxed to the O-+((6))-Mn(IV)(1)center dot structure because of the charge-spin separation for the electron-and hole-doped Mn-oxo bonds. Therefore, the local spins are responsible for the one-electron reductions of Mn(IV)(4)->Mn(III)(4) and Mn(V)(1)->Mn(IV)(1). On the other hand, the O-(5)(-) and O-(6)(+) sites generated undergo the O-O bond formation in the CaMn4O6 cluster. The Ca(II) ion in the cubane- skeleton of the CaMn4O6 cluster assists the above orbital interactions by the lowering of the orbital energy levels of pi*-LUMO of Mn(V)(1)=O-(6) and sigma*-LUMO of Mn(IV)(4)-O-(5), indicating an important role of its Lewis acidity. Present CBS mechanism for the O-O bond formation coupled with one electron reductions of