1. Microbiology and Infectious Disease
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Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division

  1. Andrew N Gray
  2. Alexander J F Egan
  3. Inge L van't Veer
  4. Jolanda Verheul
  5. Alexandre Colavin
  6. Alexandra Koumoutsi
  7. Jacob Biboy
  8. Maarten A F Altelaar
  9. Mirjam J Damen
  10. Kerwyn Casey Huang
  11. Jean-Pierre Simorre
  12. Eefjan Breukink
  13. Tanneke den Blaauwen
  14. Athanasios Typas
  15. Carol A Gross  Is a corresponding author
  16. Waldemar Vollmer
  1. University of California, San Francisco, United States
  2. Newcastle University, United Kingdom
  3. University of Utrecht, Netherlands
  4. University of Amsterdam, Netherlands
  5. Stanford University, United States
  6. European Molecular Biology Laboratory Heidelberg, Germany
  7. Université Grenoble Alpes, France
Research Article
  • Cited 71
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Cite this article as: eLife 2015;4:e07118 doi: 10.7554/eLife.07118

Abstract

To maintain cellular structure and integrity during division, Gram-negative bacteria must carefully coordinate constriction of a tripartite cell envelope of inner membrane (IM), peptidoglycan (PG) and outer membrane (OM). It has remained enigmatic how this is accomplished. Here, we show that envelope machines facilitating septal PG synthesis (PBP1B-LpoB complex) and OM constriction (Tol system) are physically and functionally coordinated via YbgF, renamed CpoB (<u><b>C</b></u>oordinator of <u><b>P</b></u>G synthesis and <u><b>O</b></u>M constriction, associated with PBP1<u><b>B</b></u>). CpoB localizes to the septum concurrent with PBP1B-LpoB and Tol at the onset of constriction, interacts with both complexes, and regulates PBP1B activity in response to Tol energy state. This coordination links PG synthesis with OM invagination and imparts a unique mode of bifunctional PG synthase regulation by selectively modulating PBP1B cross-linking activity. Coordination of the PBP1B and Tol machines by CpoB contributes to effective PBP1B function in vivo and maintenance of cell envelope integrity during division.

Article and author information

Author details

  1. Andrew N Gray

    Department of Microbiology and Immunology, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Alexander J F Egan

    Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle Upon Tyne, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Inge L van't Veer

    Membrane Biochemistry and Biophysics, Bijvoet Centre for Biomolecular Research, University of Utrecht, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Jolanda Verheul

    Bacterial Cell Biology, Swammerdam Institute for Life Sciences, Faculty of Science, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  5. Alexandre Colavin

    Biophysics Program, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Alexandra Koumoutsi

    Genome Biology Unit, European Molecular Biology Laboratory Heidelberg, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Jacob Biboy

    Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle Upon Tyne, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Maarten A F Altelaar

    Biomolecular Mass Spectrometry and Proteomics, Bijvoet Centre for Biomolecular Research, University of Utrecht, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  9. Mirjam J Damen

    Biomolecular Mass Spectrometry and Proteomics, Bijvoet Centre for Biomolecular Research, University of Utrecht, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  10. Kerwyn Casey Huang

    Biophysics Program, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Jean-Pierre Simorre

    Institut de Biologie Structurale, Université Grenoble Alpes, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
  12. Eefjan Breukink

    Membrane Biochemistry and Biophysics, Bijvoet Centre for Biomolecular Research, University of Utrecht, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  13. Tanneke den Blaauwen

    Bacterial Cell Biology, Swammerdam Institute for Life Sciences, Faculty of Science, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  14. Athanasios Typas

    Genome Biology Unit, European Molecular Biology Laboratory Heidelberg, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  15. Carol A Gross

    Department of Microbiology and Immunology, University of California, San Francisco, San Francisco, United States
    For correspondence
    cgrossucsf@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  16. Waldemar Vollmer

    Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle Upon Tyne, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Gisela Storz, National Institute of Child Health and Human Development, United States

Publication history

  1. Received: February 20, 2015
  2. Accepted: May 6, 2015
  3. Accepted Manuscript published: May 7, 2015 (version 1)
  4. Accepted Manuscript updated: May 8, 2015 (version 2)
  5. Version of Record published: June 8, 2015 (version 3)

Copyright

© 2015, Gray 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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