Theoretical insight in to hydrogen-bonding networks and proton wire for the CaMn4O5 cluster of photosystem II. Elongation of Mn-Mn distances with hydrogen bonds

M. Shoji, Hiroshi Isobe, S. Yamanaka, Yasufumi Umena, K. Kawakami, N. Kamiya, Jian-Ren Shen, K. Yamaguchi

Research output: Contribution to journalArticle

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Abstract

Quantum mechanical (QM) and QM/molecular mechanics (MM) calculations of three different cluster models have been performed to shed light on hydrogen bonding networks and proton wires for proton release pathways (PRP) of water oxidation reactions in the oxygen evolving complex (OEC) of photosystem II (PSII). Positions of all the hydrogen atoms in an extended QM Model III including the second coordination sphere for the active-site CaMn 4O5 complex of OEC of PSII have been optimized assuming the geometry of heavy atoms determined by the recent high-resolution X-ray diffraction (XRD) experiment of PSII refined to 1.9 Å resolution. Full geometry optimizations of the first coordination sphere model (QM Model I) embedded in the Model III and QM (QM Model I plus seven water molecules, namely QM Model II)/MM models, together with full QM Model III, have also been conducted to elucidate confinement effects for geometrical parameters of the CaMn4O5 cluster by proteins. Computational results by these methods have elucidated the O⋯O(N), O⋯H distances and O(N)-H⋯O angles for hydrogen bonds in proton release paths (PRP) I and II that construct a proton wire from Asp61 toward His190. The hydrogen-bonding structures revealed have also been examined in relation to the possibilities of protonation of bridge oxygen dianions within the CaMn4O5 cluster. The optimized inter-atomic distances by QM Models I and III, together with QM(Model II)/MM, have elucidated the elongation of the Mn-Mn distances with hydrogen bonds and variations of the Mnd-O(5) length with confinement effects by protein. Implications of the computational results are discussed in relation to the available EXAFS experiments, and internal, semi-internal and external reductions of Mn ions and long Mn-Mn distances of the high-resolution (SP8) XRD, and rational design of artificial catalysts for water oxidation that are current topics in the field of OEC of PSII.

Original languageEnglish
Pages (from-to)1831-1848
Number of pages18
JournalCatalysis Science and Technology
Volume3
Issue number7
DOIs
Publication statusPublished - Jul 2013

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Photosystem II Protein Complex
Protons
Elongation
Hydrogen bonds
Wire
Molecular mechanics
Oxygen
Water
Proteins
X ray diffraction
Atoms
Oxidation
Geometry
Protonation
Hydrogen
Experiments
Ions

ASJC Scopus subject areas

  • Catalysis

Cite this

Theoretical insight in to hydrogen-bonding networks and proton wire for the CaMn4O5 cluster of photosystem II. Elongation of Mn-Mn distances with hydrogen bonds. / Shoji, M.; Isobe, Hiroshi; Yamanaka, S.; Umena, Yasufumi; Kawakami, K.; Kamiya, N.; Shen, Jian-Ren; Yamaguchi, K.

In: Catalysis Science and Technology, Vol. 3, No. 7, 07.2013, p. 1831-1848.

Research output: Contribution to journalArticle

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abstract = "Quantum mechanical (QM) and QM/molecular mechanics (MM) calculations of three different cluster models have been performed to shed light on hydrogen bonding networks and proton wires for proton release pathways (PRP) of water oxidation reactions in the oxygen evolving complex (OEC) of photosystem II (PSII). Positions of all the hydrogen atoms in an extended QM Model III including the second coordination sphere for the active-site CaMn 4O5 complex of OEC of PSII have been optimized assuming the geometry of heavy atoms determined by the recent high-resolution X-ray diffraction (XRD) experiment of PSII refined to 1.9 {\AA} resolution. Full geometry optimizations of the first coordination sphere model (QM Model I) embedded in the Model III and QM (QM Model I plus seven water molecules, namely QM Model II)/MM models, together with full QM Model III, have also been conducted to elucidate confinement effects for geometrical parameters of the CaMn4O5 cluster by proteins. Computational results by these methods have elucidated the O⋯O(N), O⋯H distances and O(N)-H⋯O angles for hydrogen bonds in proton release paths (PRP) I and II that construct a proton wire from Asp61 toward His190. The hydrogen-bonding structures revealed have also been examined in relation to the possibilities of protonation of bridge oxygen dianions within the CaMn4O5 cluster. The optimized inter-atomic distances by QM Models I and III, together with QM(Model II)/MM, have elucidated the elongation of the Mn-Mn distances with hydrogen bonds and variations of the Mnd-O(5) length with confinement effects by protein. Implications of the computational results are discussed in relation to the available EXAFS experiments, and internal, semi-internal and external reductions of Mn ions and long Mn-Mn distances of the high-resolution (SP8) XRD, and rational design of artificial catalysts for water oxidation that are current topics in the field of OEC of PSII.",
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AU - Isobe, Hiroshi

AU - Yamanaka, S.

AU - Umena, Yasufumi

AU - Kawakami, K.

AU - Kamiya, N.

AU - Shen, Jian-Ren

AU - Yamaguchi, K.

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