1. Biochemistry and Chemical Biology
  2. Structural Biology and Molecular Biophysics

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
https://doi.org/10.7554/eLife.26933
Share this article
Cite this article
  1. Miao Zhang
  2. Martin Bommer
  3. Ruchira Chatterjee
  4. Rana Hussein
  5. Junko Yano
  6. Holger Dau
  7. Jan Kern
  8. Holger Dobbek
  9. Athina Zouni
(2017)
Structural insights into the light-driven auto-assembly process of the water-oxidizing Mn4CaO5-cluster in photosystem II
eLife 6:e26933.
https://doi.org/10.7554/eLife.26933
  2. Download BibTeX
  3. Download .RIS

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.

Metrics

  • 2,521
    Page views
  • 485
    Downloads
  • 48
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Miao Zhang
  2. Martin Bommer
  3. Ruchira Chatterjee
  4. Rana Hussein
  5. Junko Yano
  6. Holger Dau
  7. Jan Kern
  8. Holger Dobbek
  9. Athina Zouni
(2017)
Structural insights into the light-driven auto-assembly process of the water-oxidizing Mn4CaO5-cluster in photosystem II
eLife 6:e26933.
https://doi.org/10.7554/eLife.26933

Categories and tags

Further reading

    1. Biochemistry and Chemical Biology
    2. Chromosomes and Gene Expression

    Multiple UBX proteins reduce the ubiquitin threshold of the mammalian p97-UFD1-NPL4 unfoldase

    Ryo Fujisawa et al.
    Research Article Updated

    The p97/Cdc48 ATPase and its ubiquitin receptors Ufd1-Npl4 are essential to unfold ubiquitylated proteins in many areas of eukaryotic cell biology. In yeast, Cdc48-Ufd1-Npl4 is controlled by a quality control mechanism, whereby substrates must be conjugated to at least five ubiquitins. Here, we show that mammalian p97-UFD1-NPL4 is governed by a complex interplay between additional p97 cofactors and the number of conjugated ubiquitins. Using reconstituted assays for the disassembly of ubiquitylated CMG (Cdc45-MCM-GINS) helicase by human p97-UFD1-NPL4, we show that the unfoldase has a high ubiquitin threshold for substrate unfolding, which can be reduced by the UBX proteins UBXN7, FAF1, or FAF2. Our data indicate that the UBX proteins function by binding to p97-UFD1-NPL4 and stabilising productive interactions between UFD1-NPL4 and K48-linked chains of at least five ubiquitins. Stimulation by UBXN7 is dependent upon known ubiquitin-binding motifs, whereas FAF1 and FAF2 use a previously uncharacterised coiled-coil domain to reduce the ubiquitin threshold of p97-UFD1-NPL4. We show that deleting the Ubnx7 and Faf1 genes impairs CMG disassembly during S-phase and mitosis and sensitises cells to reduced ubiquitin ligase activity. These findings indicate that multiple UBX proteins are important for the efficient unfolding of ubiquitylated proteins by p97-UFD1-NPL4 in mammalian cells.

    1. Biochemistry and Chemical Biology
    2. Structural Biology and Molecular Biophysics

    PH domain-mediated autoinhibition and oncogenic activation of Akt

    Hwan Bae et al.
    Research Advance

    Akt is a Ser/Thr protein kinase that plays a central role in metabolism and cancer. Regulation of Akt's activity involves an autoinhibitory intramolecular interaction between its pleckstrin homology (PH) domain and its kinase domain that can be relieved by C-tail phosphorylation. PH domain mutant E17K Akt is a well-established oncogene. Previously, we reported that the conformation of autoinhibited Akt may be shifted by small molecule allosteric inhibitors limiting the mechanistic insights from existing X-ray structures that have relied on such compounds (Chu, Viennet, et al, 2020). Here we discover unexpectedly that a single mutation R86A Akt exhibits intensified autoinhibitory features with enhanced PH domain-kinase domain affinity. Structural and biochemical analysis uncovers the importance of a key interaction network involving Arg86, Glu17, and Tyr18 that controls Akt conformation and activity. Our studies also shed light on the molecular basis for E17K Akt activation as an oncogenic driver.

    1. Biochemistry and Chemical Biology
    2. Structural Biology and Molecular Biophysics

    Multi-step recognition of potential 5' splice sites by the Saccharomyces cerevisiae U1 snRNP

    Sarah R Hansen et al.
    Research Article

    In eukaryotes, splice sites define the introns of pre-mRNAs and must be recognized and excised with nucleotide precision by the spliceosome to make the correct mRNA product. In one of the earliest steps of spliceosome assembly, the U1 small nuclear ribonucleoprotein (snRNP) recognizes the 5' splice site (5' SS) through a combination of base pairing, protein-RNA contacts, and interactions with other splicing factors. Previous studies investigating the mechanisms of 5' SS recognition have largely been done in vivo or in cellular extracts where the U1/5' SS interaction is difficult to deconvolute from the effects of trans-acting factors or RNA structure. In this work we used co-localization single-molecule spectroscopy (CoSMoS) to elucidate the pathway of 5' SS selection by purified yeast U1 snRNP. We determined that U1 reversibly selects 5' SS in a sequence-dependent, two-step mechanism. A kinetic selection scheme enforces pairing at particular positions rather than overall duplex stability to achieve long-lived U1 binding. Our results provide a kinetic basis for how U1 may rapidly surveil nascent transcripts for 5' SS and preferentially accumulate at these sequences rather than on close cognates.