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
Creators: name: K. Yamaguchi
name: M. Shoji
name: H. Isobe
name: K. Miyagawa
name: K. Nakatani
Publisher: name: Taylor & Francis
Year: 2018
Subjects: subject: Biophysics
subject: Biochemistry
subject: Medicine
subject: Microbiology
subject: FOS: Biological sciences
subject: FOS: Biological sciences
subject: Cell Biology
subject: Molecular Biology
subject: Physiology
subject: Pharmacology
subject: Biotechnology
subject: Evolutionary Biology
subject: 59999 Environmental Sciences not elsewhere classified
subject: FOS: Earth and related environmental sciences
subject: FOS: Earth and related environmental sciences
subject: 39999 Chemical Sciences not elsewhere classified
subject: FOS: Chemical sciences
subject: FOS: Chemical sciences
subject: Marine Biology
subject: Inorganic Chemistry
subject: Computational Biology

description: 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<sub>4</sub> 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 σ-HOMO of the Mn(IV)<sub>4</sub>–O<sub>(5)</sub> bond and the π*-LUMO of the Mn(V)<sub>1</sub>=O<sub>(6)</sub> bond plays an important role for the concerted O–O bond formation for water oxidation in the CaMn<sub>4</sub>O<sub>6</sub> cluster of OEC of PSII. One electron transfer (OET) from the π-HOMO of the Mn(V)<sub>1</sub>=O<sub>(6)</sub> bond to the σ*-LUMO of the Mn(IV)<sub>4</sub>–O<sub>(5)</sub> bond occurs for the formation of electron transfer diradical, where the generated anion radical [Mn(IV)<sub>4</sub>–O<sub>(5)</sub>]<sup>-</sup>• part is relaxed to the •Mn(III)<sub>4</sub> … O<sub>(5)</sub><sup>-</sup> structure and the cation radical [O<sub>(6)</sub>=Mn(V)<sub>1</sub>]<sup>+</sup> • part is relaxed to the <sup>+</sup>O<sub>(6)</sub>–Mn(IV)<sub>1</sub>• 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)<sub>4</sub>-&gt;Mn(III)<sub>4</sub> and Mn(V)<sub>1</sub>-&gt;Mn(IV)<sub>1</sub>. On the other hand, the O<sub>(5)</sub><sup>-</sup> and O<sub>(6)</sub><sup>+</sup> sites generated undergo the O–O bond formation in the CaMn<sub>4</sub>O<sub>6</sub> cluster. The Ca(II) ion in the cubane- skeleton of the CaMn<sub>4</sub>O<sub>6</sub> cluster assists the above orbital interactions by the lowering of the orbital energy levels of π*-LUMO of Mn(V)<sub>1</sub>=O<sub>(6)</sub> and σ*-LUMO of Mn(IV)<sub>4</sub>–O<sub>(5)</sub>, indicating an important role of its Lewis acidity. Present CBS mechanism for the O–O bond formation coupled with one electron reductions of the high-valent Mn ions is different from the conventional radical coupling (RC) and acid-base (AB) mechanisms for water oxidation in artificial and native photosynthesis systems. The proton-coupled electron transfer (PC-OET) mechanism for the O–O bond formation is also touched in relation to the CBS-OET mechanism.