Concerted Mechanism of Water Insertion and O2 Release during the S4 to S0 Transition of the Oxygen-Evolving Complex in Photosystem II

Mitsuo Shoji, Hiroshi Isobe, Yasuteru Shigeta, Takahito Nakajima, Kizashi Yamaguchi

Research output: Contribution to journalArticlepeer-review

23 Citations (Scopus)


The O2 release of the oxygen-evolving complex of the photosystem II (PSII) is one of the essential processes responsible for the highly efficient O2 production. Despite its importance, the detailed molecular mechanism is still unsolved. In the present study, we show that the O2 release is directly coupled with water insertion into the Mn cluster based on the quantum mechanics/molecular mechanics (QM/MM) calculations. In this mechanism, the O2 molecule first dissociates from the Mn sites in order, that is, the O atom coordinating to the Mn3 (O5a) first dissociates, then the other O atom coordinating to the Mn1 (O5d) dissociates in the next step in the late S4 state (1 → 2). Next, the O2 migrates to a space surrounded by the Val185 and His332 side chains as one water molecule coordinating to the Ca2+ ion (W3) comes into the O2 bonded site (2 → 3). Finally, a pre-S0 state (4) is formed after a proton transfer from the inserted water to the other proton acceptor site (W2) (3 → 4). The highest activation barrier during these reactions was found at the O2 release step (2 → 3) that only requires E = 12.7 kcal mol-1 (G = 10.4 kcal mol-1). A series of the reactions (2 → 3) look like a chain crash of billiard balls because the W3 is inserted into the catalytic center from the water-abundant side (Ca2+ ion side), and then the O2 moiety is pushed out to the opposite side (Val185 side). The hydrophobic residue of Val185 covers the active O5 site and forms an O2-specific permeation tunnel. The present sequential reactions clearly demonstrate the efficient removal of the toxic O2 from the catalytic center and implications of the essential roles of Val185, Ca2+ ions and water molecules, which are all present in the active site of PSII as the indispensable constituents.

Original languageEnglish
Pages (from-to)6491-6502
Number of pages12
JournalJournal of Physical Chemistry B
Issue number25
Publication statusPublished - Jun 28 2018

ASJC Scopus subject areas

  • Physical and Theoretical Chemistry
  • Surfaces, Coatings and Films
  • Materials Chemistry


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