Proton transfer pathway from the oxygen-evolving complex in photosystem II substantiated by extensive mutagenesis

Hiroshi Kuroda, Keisuke Kawashima, Kazuyo Ueda, Takuya Ikeda, Keisuke Saito, Ryo Ninomiya, Chisato Hida, Yuichiro Takahashi, Hiroshi Ishikita

    Research output: Contribution to journalArticlepeer-review

    4 Citations (Scopus)

    Abstract

    We report a structure-based biological approach to identify the proton-transfer pathway in photosystem II. First, molecular dynamics (MD) simulations were conducted to analyze the H-bond network that may serve as a Grotthuss-like proton conduit. MD simulations show that D1-Asp61, the H-bond acceptor of H2O at the Mn4CaO5 cluster (W1), forms an H-bond via one water molecule with D1-Glu65 but not with D2-Glu312. Then, D1-Asp61, D1-Glu65, D2-Glu312, and the adjacent residues, D1-Arg334, D2-Glu302, and D2-Glu323, were thoroughly mutated to the other 19 residues, i.e., 114 Chlamydomonas chloroplast mutant cells were generated. Mutation of D1-Asp61 was most crucial. Only the D61E and D61C cells grew photoautotrophically and exhibit O2-evolving activity. Mutations of D2-Glu312 were less crucial to photosynthetic growth than mutations of D1-Glu65. Quantum mechanical/molecular mechanical calculations indicated that in the PSII crystal structure, the proton is predominantly localized at D1-Glu65 along the H-bond with D2-Glu312, i.e., pKa(D1-Glu65) > pKa(D2-Glu312). The potential-energy profile shows that the release of the proton from D1-Glu65 leads to the formation of the two short H-bonds between D1-Asp61 and D1-Glu65, which facilitates downhill proton transfer along the Grotthuss-like proton conduit in the S2 to S3 transition. It seems possible that D1-Glu65 is involved in the dominant pathway that proceeds from W1 via D1-Asp61 toward the thylakoid lumen, whereas D2-Glu312 and D1-Arg334 may be involved in alternative pathways in some mutants.

    Original languageEnglish
    Article number148329
    JournalBiochimica et Biophysica Acta - Bioenergetics
    Volume1862
    Issue number1
    DOIs
    Publication statusPublished - Jan 1 2021

    Keywords

    • Molecular dynamics simulations
    • Oxygen-evolving activity
    • Photosystem II
    • Proton transfer pathway
    • Quantum mechanical/molecular mechanical calculations

    ASJC Scopus subject areas

    • Biophysics
    • Biochemistry
    • Cell Biology

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