Assembling the Tat protein translocase

  1. Felicity Alcock
  2. Phillip J Stansfeld  Is a corresponding author
  3. Hajra Basit
  4. Johann Habersetzer
  5. Matthew AB Baker
  6. Tracy Palmer
  7. Mark I Wallace
  8. Ben C Berks  Is a corresponding author
  1. University of Oxford, United Kingdom
  2. Kings College London, United Kingdom
  3. University of Dundee, United Kingdom
  4. University of New South Wales, Australia

Abstract

The twin-arginine protein translocation system (Tat) transports folded proteins across the bacterial cytoplasmic membrane and the thylakoid membranes of plant chloroplasts. The Tat transporter is assembled from multiple copies of the membrane proteins TatA, TatB, and TatC. We combine sequence co-evolution analysis, molecular simulations, and experimentation to define the interactions between the Tat proteins of Escherichia coli at molecular-level resolution. In the TatBC receptor complex the transmembrane helix of each TatB molecule is sandwiched between two TatC molecules, with one of the inter-subunit interfaces incorporating a functionally important cluster of interacting polar residues. Unexpectedly, we find that TatA also associates with TatC at the polar cluster site. Our data provide a structural model for assembly of the active Tat translocase in which substrate binding triggers replacement of TatB by TatA at the polar cluster site. Our work demonstrates the power of co-evolution analysis to predict protein interfaces in multi-subunit complexes.

Article and author information

Author details

  1. Felicity Alcock

    Department of Biochemistry, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Phillip J Stansfeld

    Department of Biochemistry, University of Oxford, Oxford, United Kingdom
    For correspondence
    phillip.stansfeld@bioch.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  3. Hajra Basit

    Department of Chemistry, Kings College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Johann Habersetzer

    Division of Molecular Microbiology, College of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Matthew AB Baker

    EMBL Australia Node for Single Molecule Science, University of New South Wales, Kensington, Australia
    Competing interests
    The authors declare that no competing interests exist.
  6. Tracy Palmer

    Division of Molecular Microbiology, College of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Mark I Wallace

    Department of Chemistry, Kings College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5692-8313
  8. Ben C Berks

    Department of Biochemistry, University of Oxford, Oxford, United Kingdom
    For correspondence
    ben.berks@bioch.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9685-4067

Funding

Biotechnology and Biological Sciences Research Council (BB/L002531/1)

  • Tracy Palmer
  • Ben C Berks

Wellcome (Investigator Award 107929/Z/15/Z)

  • Ben C Berks

Medical Research Council (G1001640)

  • Tracy Palmer
  • Ben C Berks

European Commission (Marie Curie Fellowship Programme: GP7-PEOPLE-2013-IEF 626436)

  • Hajra Basit
  • Mark I Wallace

Biotechnology and Biological Sciences Research Council (BB/I019855/1)

  • Phillip J Stansfeld

Wellcome (Investigator Award 110183/Z/15/Z)

  • Tracy Palmer

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Nir Ben-Tal, Tel Aviv University, Israel

Publication history

  1. Received: August 22, 2016
  2. Accepted: November 29, 2016
  3. Accepted Manuscript published: December 3, 2016 (version 1)
  4. Accepted Manuscript updated: December 16, 2016 (version 2)
  5. Accepted Manuscript updated: December 20, 2016 (version 3)
  6. Version of Record published: December 30, 2016 (version 4)

Copyright

© 2016, Alcock 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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  1. Felicity Alcock
  2. Phillip J Stansfeld
  3. Hajra Basit
  4. Johann Habersetzer
  5. Matthew AB Baker
  6. Tracy Palmer
  7. Mark I Wallace
  8. Ben C Berks
(2016)
Assembling the Tat protein translocase
eLife 5:e20718.
https://doi.org/10.7554/eLife.20718
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