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Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition

Author

Listed:
  • Rana Hussein

    (Institut für Biologie, Humboldt-Universität zu Berlin)

  • Mohamed Ibrahim

    (Institut für Biologie, Humboldt-Universität zu Berlin)

  • Asmit Bhowmick

    (Lawrence Berkeley National Laboratory)

  • Philipp S. Simon

    (Lawrence Berkeley National Laboratory)

  • Ruchira Chatterjee

    (Lawrence Berkeley National Laboratory)

  • Louise Lassalle

    (Lawrence Berkeley National Laboratory)

  • Margaret Doyle

    (Lawrence Berkeley National Laboratory)

  • Isabel Bogacz

    (Lawrence Berkeley National Laboratory)

  • In-Sik Kim

    (Lawrence Berkeley National Laboratory)

  • Mun Hon Cheah

    (Uppsala University)

  • Sheraz Gul

    (Lawrence Berkeley National Laboratory)

  • Casper Lichtenberg

    (Uppsala University
    Umeå University)

  • Petko Chernev

    (Uppsala University)

  • Cindy C. Pham

    (Lawrence Berkeley National Laboratory)

  • Iris D. Young

    (Lawrence Berkeley National Laboratory)

  • Sergio Carbajo

    (Linac Coherent Light Source, SLAC National Accelerator Laboratory)

  • Franklin D. Fuller

    (Linac Coherent Light Source, SLAC National Accelerator Laboratory)

  • Roberto Alonso-Mori

    (Linac Coherent Light Source, SLAC National Accelerator Laboratory)

  • Alex Batyuk

    (Linac Coherent Light Source, SLAC National Accelerator Laboratory)

  • Kyle D. Sutherlin

    (Lawrence Berkeley National Laboratory)

  • Aaron S. Brewster

    (Lawrence Berkeley National Laboratory)

  • Robert Bolotovsky

    (Lawrence Berkeley National Laboratory)

  • Derek Mendez

    (Lawrence Berkeley National Laboratory)

  • James M. Holton

    (Lawrence Berkeley National Laboratory)

  • Nigel W. Moriarty

    (Lawrence Berkeley National Laboratory)

  • Paul D. Adams

    (Lawrence Berkeley National Laboratory
    University of California)

  • Uwe Bergmann

    (University of Wisconsin–Madison)

  • Nicholas K. Sauter

    (Lawrence Berkeley National Laboratory)

  • Holger Dobbek

    (Institut für Biologie, Humboldt-Universität zu Berlin)

  • Johannes Messinger

    (Uppsala University
    Umeå University)

  • Athina Zouni

    (Institut für Biologie, Humboldt-Universität zu Berlin)

  • Jan Kern

    (Lawrence Berkeley National Laboratory)

  • Vittal K. Yachandra

    (Lawrence Berkeley National Laboratory)

  • Junko Yano

    (Lawrence Berkeley National Laboratory)

Abstract

Light-driven oxidation of water to molecular oxygen is catalyzed by the oxygen-evolving complex (OEC) in Photosystem II (PS II). This multi-electron, multi-proton catalysis requires the transport of two water molecules to and four protons from the OEC. A high-resolution 1.89 Å structure obtained by averaging all the S states and refining the data of various time points during the S2 to S3 transition has provided better visualization of the potential pathways for substrate water insertion and proton release. Our results indicate that the O1 channel is the likely water intake pathway, and the Cl1 channel is the likely proton release pathway based on the structural rearrangements of water molecules and amino acid side chains along these channels. In particular in the Cl1 channel, we suggest that residue D1-E65 serves as a gate for proton transport by minimizing the back reaction. The results show that the water oxidation reaction at the OEC is well coordinated with the amino acid side chains and the H-bonding network over the entire length of the channels, which is essential in shuttling substrate waters and protons.

Suggested Citation

  • Rana Hussein & Mohamed Ibrahim & Asmit Bhowmick & Philipp S. Simon & Ruchira Chatterjee & Louise Lassalle & Margaret Doyle & Isabel Bogacz & In-Sik Kim & Mun Hon Cheah & Sheraz Gul & Casper Lichtenber, 2021. "Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26781-z
    DOI: 10.1038/s41467-021-26781-z
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    References listed on IDEAS

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    2. Iris D. Young & Mohamed Ibrahim & Ruchira Chatterjee & Sheraz Gul & Franklin D. Fuller & Sergey Koroidov & Aaron S. Brewster & Rosalie Tran & Roberto Alonso-Mori & Thomas Kroll & Tara Michels-Clark & , 2016. "Structure of photosystem II and substrate binding at room temperature," Nature, Nature, vol. 540(7633), pages 453-457, December.
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    6. Jan Kern & Ruchira Chatterjee & Iris D. Young & Franklin D. Fuller & Louise Lassalle & Mohamed Ibrahim & Sheraz Gul & Thomas Fransson & Aaron S. Brewster & Roberto Alonso-Mori & Rana Hussein & Miao Zh, 2018. "Structures of the intermediates of Kok’s photosynthetic water oxidation clock," Nature, Nature, vol. 563(7731), pages 421-425, November.
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    Cited by:

    1. Yu Guo & Lanlan He & Yunxuan Ding & Lars Kloo & Dimitrios A. Pantazis & Johannes Messinger & Licheng Sun, 2024. "Closing Kok’s cycle of nature’s water oxidation catalysis," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Ziyu Zhao & Irene Vercellino & Jana Knoppová & Roman Sobotka & James W. Murray & Peter J. Nixon & Leonid A. Sazanov & Josef Komenda, 2023. "The Ycf48 accessory factor occupies the site of the oxygen-evolving manganese cluster during photosystem II biogenesis," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

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