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

K. Yamaguchi, M. Shoji, Hiroshi Isobe, K. Miyagawa, K. Nakatani

Research output: Contribution to journalArticle

Abstract

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 S4 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)4–O(5) bond and the π*-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 π-HOMO of the Mn(V)1=O(6) bond to the σ*-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)]-• part is relaxed to the •Mn(III)4 … O(5) - structure and the cation radical [O(6)=Mn(V)1]+ • part is relaxed to the +O(6)–Mn(IV)1• 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 π*-LUMO of Mn(V)1=O(6) and σ*-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 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.

Original languageEnglish
JournalMolecular Physics
DOIs
Publication statusAccepted/In press - Jan 1 2018

Fingerprint

Photosystem II Protein Complex
Chemical bonds
chemical bonds
electron transfer
Electrons
Oxygen
Oxidation
oxidation
Water
oxygen
water
orbitals
cubane
Ions
electrons
photosynthesis
Photosynthesis
musculoskeletal system
acidity
occupation

Keywords

  • Concerted bond switching (CBS)
  • OEC
  • one electron transfer (OET)
  • O–O bond formation
  • PSII
  • transition state (TS)
  • water oxidation

ASJC Scopus subject areas

  • Biophysics
  • Molecular Biology
  • Condensed Matter Physics
  • Physical and Theoretical Chemistry

Cite this

@article{caeb6c54f7ea489bab02720c14bd93cd,
title = "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",
abstract = "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 S4 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)4–O(5) bond and the π*-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 π-HOMO of the Mn(V)1=O(6) bond to the σ*-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)]-• part is relaxed to the •Mn(III)4 … O(5) - structure and the cation radical [O(6)=Mn(V)1]+ • part is relaxed to the +O(6)–Mn(IV)1• 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 π*-LUMO of Mn(V)1=O(6) and σ*-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 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.",
keywords = "Concerted bond switching (CBS), OEC, one electron transfer (OET), O–O bond formation, PSII, transition state (TS), water oxidation",
author = "K. Yamaguchi and M. Shoji and Hiroshi Isobe and K. Miyagawa and K. Nakatani",
year = "2018",
month = "1",
day = "1",
doi = "10.1080/00268976.2018.1552799",
language = "English",
journal = "Molecular Physics",
issn = "0026-8976",
publisher = "Taylor and Francis Ltd.",

}

TY - JOUR

T1 - Theory of chemical bonds in metalloenzymes XXII

T2 - 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

AU - Yamaguchi, K.

AU - Shoji, M.

AU - Isobe, Hiroshi

AU - Miyagawa, K.

AU - Nakatani, K.

PY - 2018/1/1

Y1 - 2018/1/1

N2 - 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 S4 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)4–O(5) bond and the π*-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 π-HOMO of the Mn(V)1=O(6) bond to the σ*-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)]-• part is relaxed to the •Mn(III)4 … O(5) - structure and the cation radical [O(6)=Mn(V)1]+ • part is relaxed to the +O(6)–Mn(IV)1• 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 π*-LUMO of Mn(V)1=O(6) and σ*-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 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.

AB - 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 S4 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)4–O(5) bond and the π*-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 π-HOMO of the Mn(V)1=O(6) bond to the σ*-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)]-• part is relaxed to the •Mn(III)4 … O(5) - structure and the cation radical [O(6)=Mn(V)1]+ • part is relaxed to the +O(6)–Mn(IV)1• 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 π*-LUMO of Mn(V)1=O(6) and σ*-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 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.

KW - Concerted bond switching (CBS)

KW - OEC

KW - one electron transfer (OET)

KW - O–O bond formation

KW - PSII

KW - transition state (TS)

KW - water oxidation

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