### Abstract

In order to confirm theoretical system models of photosystem II (PSII), quantum mechanics (QM)/molecular mechanics (MM) calculations using a large-scale QM model (QM Model V) have been performed to elucidate hydrogen bonding networks and proton wires for proton release pathways (PRPs) of water oxidation reaction in the oxygen-evolving complex (OEC) of PSII. Full geometry optimizations of PRP by the QM/MM model have been carried out starting from the geometry of heavy atoms determined by the recent high-resolution X-ray diffraction (XRD) experiment on PSII refined to 1.9Å resolution. The optimized MnMn and CaMn distances by large-scale QM/MM are consistent with the EXAFS results, removing out the discrepancy between the refined XRD and EXAFS. Computational results from QM/MM calculations have demonstrated the labile nature of the Mn_{a}O_{(5)}Mn_{d} bond of the CaMn_{4}O_{5} cluster in the OEC of PSII which allows left (L)-opened, quasi-central (C_{Q})-, and right (R)-opened structures. This confirms the feasibility of the left- and right-hand scenarios for water oxidation in the OEC of PSII that are dependent on the hydrogen bonding networks. The QM/MM computations have elucidated the networks structures: hydrogen bonding O. . .O(N) and O. . .H distances and O(N)H. . .O angles in PRP, together with the ClO(N) and Cl. . .H distances and O(N)H. . .Cl angles for chloride anions. The obtained hydrogen bonding networks are fully consistent with the results from XRD and available experiments such as EXAFS, showing the reliability of our theoretical system model that is crucial for investigations of functions of PSII such as water oxidation. The QM/MM computations have elucidated possible roles of chloride anions in OEC of PSII for proton transfers. The QM/MM computational results have provided useful information for the understanding and explanation of several experimental results obtained with mutants of the OEC of PSII. The possible implications of the present results are discussed in relation to our theoretical system models of PSII, strong or weak perturbations of the system structures by mutations, damage-free X-ray free-electron laser structure of PSII, and bioinspired working hypotheses for the development of artificial water oxidation systems which use 3d transition metal complexes.

Original language | English |
---|---|

Pages (from-to) | 325-413 |

Number of pages | 89 |

Journal | Advances in Quantum Chemistry |

Volume | 70 |

DOIs | |

Publication status | Published - 2015 |

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### Keywords

- Hydrogen bonding networks
- Oxygen-evolving complex
- Photosystem II
- Proton transfer pathway
- QM/MM calculation
- Theoretical system model
- Water inlet channel
- Water oxidation

### ASJC Scopus subject areas

- Physical and Theoretical Chemistry

### Cite this

*Advances in Quantum Chemistry*,

*70*, 325-413. https://doi.org/10.1016/bs.aiq.2014.10.001

**Large-Scale QM/MM Calculations of Hydrogen Bonding Networks for Proton Transfer and Water Inlet Channels for Water Oxidation-Theoretical System Models of the Oxygen-Evolving Complex of Photosystem II.** / Shoji, M.; Isobe, Hiroshi; Yamanaka, S.; Umena, Yasufumi; Kawakami, K.; Kamiya, N.; Shen, Jian-Ren; Nakajima, T.; Yamaguchi, K.

Research output: Contribution to journal › Article

*Advances in Quantum Chemistry*, vol. 70, pp. 325-413. https://doi.org/10.1016/bs.aiq.2014.10.001

}

TY - JOUR

T1 - Large-Scale QM/MM Calculations of Hydrogen Bonding Networks for Proton Transfer and Water Inlet Channels for Water Oxidation-Theoretical System Models of the Oxygen-Evolving Complex of Photosystem II

AU - Shoji, M.

AU - Isobe, Hiroshi

AU - Yamanaka, S.

AU - Umena, Yasufumi

AU - Kawakami, K.

AU - Kamiya, N.

AU - Shen, Jian-Ren

AU - Nakajima, T.

AU - Yamaguchi, K.

PY - 2015

Y1 - 2015

N2 - In order to confirm theoretical system models of photosystem II (PSII), quantum mechanics (QM)/molecular mechanics (MM) calculations using a large-scale QM model (QM Model V) have been performed to elucidate hydrogen bonding networks and proton wires for proton release pathways (PRPs) of water oxidation reaction in the oxygen-evolving complex (OEC) of PSII. Full geometry optimizations of PRP by the QM/MM model have been carried out starting from the geometry of heavy atoms determined by the recent high-resolution X-ray diffraction (XRD) experiment on PSII refined to 1.9Å resolution. The optimized MnMn and CaMn distances by large-scale QM/MM are consistent with the EXAFS results, removing out the discrepancy between the refined XRD and EXAFS. Computational results from QM/MM calculations have demonstrated the labile nature of the MnaO(5)Mnd bond of the CaMn4O5 cluster in the OEC of PSII which allows left (L)-opened, quasi-central (CQ)-, and right (R)-opened structures. This confirms the feasibility of the left- and right-hand scenarios for water oxidation in the OEC of PSII that are dependent on the hydrogen bonding networks. The QM/MM computations have elucidated the networks structures: hydrogen bonding O. . .O(N) and O. . .H distances and O(N)H. . .O angles in PRP, together with the ClO(N) and Cl. . .H distances and O(N)H. . .Cl angles for chloride anions. The obtained hydrogen bonding networks are fully consistent with the results from XRD and available experiments such as EXAFS, showing the reliability of our theoretical system model that is crucial for investigations of functions of PSII such as water oxidation. The QM/MM computations have elucidated possible roles of chloride anions in OEC of PSII for proton transfers. The QM/MM computational results have provided useful information for the understanding and explanation of several experimental results obtained with mutants of the OEC of PSII. The possible implications of the present results are discussed in relation to our theoretical system models of PSII, strong or weak perturbations of the system structures by mutations, damage-free X-ray free-electron laser structure of PSII, and bioinspired working hypotheses for the development of artificial water oxidation systems which use 3d transition metal complexes.

AB - In order to confirm theoretical system models of photosystem II (PSII), quantum mechanics (QM)/molecular mechanics (MM) calculations using a large-scale QM model (QM Model V) have been performed to elucidate hydrogen bonding networks and proton wires for proton release pathways (PRPs) of water oxidation reaction in the oxygen-evolving complex (OEC) of PSII. Full geometry optimizations of PRP by the QM/MM model have been carried out starting from the geometry of heavy atoms determined by the recent high-resolution X-ray diffraction (XRD) experiment on PSII refined to 1.9Å resolution. The optimized MnMn and CaMn distances by large-scale QM/MM are consistent with the EXAFS results, removing out the discrepancy between the refined XRD and EXAFS. Computational results from QM/MM calculations have demonstrated the labile nature of the MnaO(5)Mnd bond of the CaMn4O5 cluster in the OEC of PSII which allows left (L)-opened, quasi-central (CQ)-, and right (R)-opened structures. This confirms the feasibility of the left- and right-hand scenarios for water oxidation in the OEC of PSII that are dependent on the hydrogen bonding networks. The QM/MM computations have elucidated the networks structures: hydrogen bonding O. . .O(N) and O. . .H distances and O(N)H. . .O angles in PRP, together with the ClO(N) and Cl. . .H distances and O(N)H. . .Cl angles for chloride anions. The obtained hydrogen bonding networks are fully consistent with the results from XRD and available experiments such as EXAFS, showing the reliability of our theoretical system model that is crucial for investigations of functions of PSII such as water oxidation. The QM/MM computations have elucidated possible roles of chloride anions in OEC of PSII for proton transfers. The QM/MM computational results have provided useful information for the understanding and explanation of several experimental results obtained with mutants of the OEC of PSII. The possible implications of the present results are discussed in relation to our theoretical system models of PSII, strong or weak perturbations of the system structures by mutations, damage-free X-ray free-electron laser structure of PSII, and bioinspired working hypotheses for the development of artificial water oxidation systems which use 3d transition metal complexes.

KW - Hydrogen bonding networks

KW - Oxygen-evolving complex

KW - Photosystem II

KW - Proton transfer pathway

KW - QM/MM calculation

KW - Theoretical system model

KW - Water inlet channel

KW - Water oxidation

UR - http://www.scopus.com/inward/record.url?scp=84923102137&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84923102137&partnerID=8YFLogxK

U2 - 10.1016/bs.aiq.2014.10.001

DO - 10.1016/bs.aiq.2014.10.001

M3 - Article

AN - SCOPUS:84923102137

VL - 70

SP - 325

EP - 413

JO - Advances in Quantum Chemistry

JF - Advances in Quantum Chemistry

SN - 0065-3276

ER -