1. Biochemistry and Chemical Biology
  2. Structural Biology and Molecular Biophysics
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Structural insights into the light-driven auto-assembly process of the water-oxidizing Mn4CaO5-cluster in photosystem II

  1. Miao Zhang
  2. Martin Bommer
  3. Ruchira Chatterjee
  4. Rana Hussein
  5. Junko Yano
  6. Holger Dau  Is a corresponding author
  7. Jan Kern  Is a corresponding author
  8. Holger Dobbek
  9. Athina Zouni  Is a corresponding author
  1. Humboldt-Universität zu Berlin, Germany
  2. Max-Delbrück-Center for Molecular Medicine, Germany
  3. Lawrence Berkeley National Laboratory, United States
  4. Freie Universität Berlin, Germany
Research Article
  • Cited 36
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Cite this article as: eLife 2017;6:e26933 doi: 10.7554/eLife.26933

Abstract

In plants, algae and cyanobacteria, Photosystem II (PSII) catalyzes the light-driven splitting of water at a protein-bound Mn4CaO5-cluster, the water-oxidizing complex (WOC). In the photosynthetic organisms, the light-driven formation of the WOC from dissolved metal ions is a key process because it is essential in both initial activation and continuous repair of PSII. Structural information is required for understanding of this chaperone-free metal-cluster assembly. For the first time, we obtained a structure of PSII from Thermosynechococcus elongatus without the Mn4CaO5-cluster. Surprisingly, cluster-removal leaves the positions of all coordinating amino acid residues and most nearby water molecules largely unaffected, resulting in a pre-organized ligand shell for kinetically competent and error-free photo-assembly of the Mn4CaO5-cluster. First experiments initiating (i) partial disassembly and (ii) partial re-assembly after complete depletion of the Mn4CaO5-cluster agree with a specific bi-manganese cluster, likely a di-µ-oxo bridged pair of Mn(III) ions, as an assembly intermediate.

Article and author information

Author details

  1. Miao Zhang

    Institut für Biologie, Humboldt-Universität zu Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Martin Bommer

    Max-Delbrück-Center for Molecular Medicine, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Ruchira Chatterjee

    Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Rana Hussein

    Institut für Biologie, Humboldt-Universität zu Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Junko Yano

    Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Holger Dau

    Freie Universität Berlin, Berlin, Germany
    For correspondence
    holger.dau@fu-berlin.de
    Competing interests
    The authors declare that no competing interests exist.
  7. Jan Kern

    Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, United States
    For correspondence
    jfkern@lbl.gov
    Competing interests
    The authors declare that no competing interests exist.
  8. Holger Dobbek

    Institut für Biologie, Humboldt-Universität zu Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4122-3898
  9. Athina Zouni

    Institut für Biologie, Humboldt-Universität zu Berlin, Berlin, Germany
    For correspondence
    athina.zouni@hu-berlin.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0561-6990

Funding

Human Frontier Science Program (Project Award No. RGP0063/2013 310)

  • Rana Hussein

Human Frontier Science Program (Project Award No. RGP0063/2013 310)

  • Junko Yano

Human Frontier Science Program (Project Award No. RGP0063/2013 310)

  • Athina Zouni

National Institutes of Health (GM055302)

  • Ruchira Chatterjee
  • Jan Kern

Deutsche Forschungsgemeinschaft Unifying Concepts in Catalysis (Project E3)

  • Miao Zhang
  • Holger Dau
  • Holger Dobbek

Deutsche Forschungsgemeinschaft Sonderforschungsbereich 1078 (Project A5)

  • Holger Dau
  • Holger Dobbek
  • Athina Zouni

Deutsche Forschungsgemeinschaft Sonderforschungbereich 1078 (Project A4)

  • Martin Bommer

Biosciences of the Department of Energy (Contact number: DE-AC02-05CH11231)

  • Junko Yano
  • Jan Kern

Only Human Frontier Science Program (HFSP) can be found in the funder list .The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Paul G Falkowski, Rutgers University, United States

Publication history

  1. Received: March 17, 2017
  2. Accepted: July 17, 2017
  3. Accepted Manuscript published: July 18, 2017 (version 1)
  4. Version of Record published: August 3, 2017 (version 2)

Copyright

© 2017, Zhang et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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