Theory of chemical bonds in metalloenzymes XXI. Possible mechanisms of water oxidation in oxygen evolving complex of photosystem II

Kizashi Yamaguchi, Mitsuo Shoji, Hiroshi Isobe, Shusuke Yamanaka, Takashi Kawakami, Satoru Yamada, Michio Katouda, Takahito Nakajima

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30 Citations (Scopus)


Possible mechanisms for water cleavage in oxygen evolving complex (OEC) of photosystem II (PSII) have been investigated based on broken-symmetry (BS) hybrid DFT (HDFT)/def2 TZVP calculations in combination with available XRD, XFEL, EXAFS, XES and EPR results. The BS HDFT and the experimental results have provided basic concepts for understanding of chemical bonds of the CaMn4O5 cluster in the catalytic site of OEC of PSII for elucidation of the mechanism of photosynthetic water cleavage. Scope and applicability of the hybrid DFT (HDFT) methods have been examined in relation to relative stabilities of possible nine intermediates such as Mn-hydroxide, Mn-oxo, Mn-peroxo, Mn-superoxo, etc., in order to understand the O–O (O–OH) bond formation in the S3 and/or S4 states of OEC of PSII. The relative stabilities among these intermediates are variable, depending on the weight of the Hartree–Fock exchange term of HDFT. The Mn-hydroxide, Mn-oxo and Mn-superoxo intermediates are found to be preferable in the weak, intermediate and strong electron correlation regimes, respectively. Recent different serial femtosecond X-ray (SFX) results in the S3 state are investigated based on the proposed basic concepts under the assumption of different water-insertion steps for water cleavage in the Kok cycle. The observation of water insertion in the S3 state is compatible with previous large-scale QM/MM results and previous theoretical proposal for the chemical equilibrium mechanism in the S3 state. On the other hand, the no detection of water insertion in the S3 state based on other SFX results is consistent with previous proposal of the O–OH (or O–O) bond formation in the S4 state. Radical coupling and non-adiabatic one-electron transfer (NA-OET) mechanisms for the OO-bond formation are examined using the energy diagrams by QM calculations and by QM(UB3LYP)/MM calculations. Possible reaction pathways for the O–O and O–OH bond formations are also investigated based on two water-inlet pathways for oxygen evolution in OEC of PSII. Future perspectives are discussed in relation to post HDFT calculations of the energy diagrams for elucidation of the mechanism of water oxidation in OEC of PSII.

Original languageEnglish
Pages (from-to)717-745
Number of pages29
JournalMolecular Physics
Issue number5-6
Publication statusPublished - Mar 19 2018


  • CaMn4O5 cluster
  • OEC of PSII
  • Water oxidation
  • hybrid DFT/def2 TZVP
  • reaction mechanism

ASJC Scopus subject areas

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


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