1. Biochemistry and Chemical Biology
  2. Microbiology and Infectious Disease
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A unifying mechanism for the biogenesis of membrane proteins co-operatively integrated by the Sec and Tat pathways

  1. Fiona J Tooke
  2. Marion Babot
  3. Govind Chandra
  4. Grant Buchanan
  5. Tracy Palmer  Is a corresponding author
  1. University of Dundee, United Kingdom
  2. John Innes Centre, United Kingdom
Research Article
  • Cited 3
  • Views 1,790
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Cite this article as: eLife 2017;6:e26577 doi: 10.7554/eLife.26577

Abstract

The majority of multi-spanning membrane proteins are co-translationally inserted into the bilayer by the Sec pathway. An important subset of membrane proteins have globular, cofactor-containing extracytoplasmic domains requiring the dual action of the co-translational Sec and post-translational Tat pathways for integration. Here, we identify further unexplored families of membrane proteins that are dual Sec-Tat-targeted. We establish that a predicted heme-molybdenum cofactor-containing protein, and a complex polyferredoxin, each require the concerted action of two translocases for their assembly. We determine that the mechanism of handover from Sec to Tat pathway requires the relatively low hydrophobicity of the Tat-dependent transmembrane domain. This, coupled with the presence of C-terminal positive charges, results in abortive insertion of this transmembrane domain by the Sec pathway and its subsequent release at the cytoplasmic side of the membrane. Together, our data points to a simple unifying mechanism governing the assembly of dual targeted membrane proteins.

Article and author information

Author details

  1. Fiona J Tooke

    Division of Molecular Microbiology, School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Marion Babot

    Division of Molecular Microbiology, School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Govind Chandra

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Grant Buchanan

    Division of Molecular Microbiology, School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Tracy Palmer

    Division of Molecular Microbiology, School of Life Sciences, University of Dundee, Dundee, United Kingdom
    For correspondence
    t.palmer@dundee.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9043-2592

Funding

Biotechnology and Biological Sciences Research Council (BB/L000768/1)

  • Marion Babot
  • Grant Buchanan

Medical Research Council (MR/K500896/1)

  • Fiona J Tooke

Biotechnology and Biological Sciences Research Council (BB/J004561/1)

  • Govind Chandra

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

Reviewing Editor

  1. Reid Gilmore, University of Massachusetts Medical School, United States

Publication history

  1. Received: March 7, 2017
  2. Accepted: May 15, 2017
  3. Accepted Manuscript published: May 17, 2017 (version 1)
  4. Version of Record published: May 30, 2017 (version 2)

Copyright

© 2017, Tooke 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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