MreB filaments align along greatest principal membrane curvature to orient cell wall synthesis

  1. Saman Hussain
  2. Carl N Wivagg
  3. Piotr Szwedziak
  4. Felix Wong
  5. Kaitlin Schaefer
  6. Thierry Izoré
  7. Lars D Renner
  8. Matthew J Holmes
  9. Yingjie Sun
  10. Alexandre W Bisson-Filho
  11. Suzanne Walker
  12. Ariel Amir
  13. Jan Löwe
  14. Ethan C Garner  Is a corresponding author
  1. Harvard University, United States
  2. MRC Laboratory of Molecular Biology, United Kingdom
  3. Harvard John A. Paulson School of Engineering and Applied Sciences, United States
  4. Leibniz Institute of Polymer Research, Germany

Abstract

MreB is essential for rod shape in many bacteria. Membrane-associated MreB filaments move around the rod circumference, helping to insert cell wall in the radial direction to reinforce rod shape. To understand how oriented MreB motion arises, we altered the shape of Bacillus subtilis. MreB motion is isotropic in round cells, and orientation is restored when rod shape is externally imposed. Stationary filaments orient within protoplasts, and purified MreB tubulates liposomes in vitro, orienting within tubes. Together, this demonstrates MreB orients along the greatest principal membrane curvature, a conclusion supported with biophysical modeling. We observed that spherical cells regenerate into rods in a local, self-reinforcing manner: rapidly propagating rods emerge from small bulges, exhibiting oriented MreB motion. We propose that the coupling of MreB filament alignment to shape-reinforcing peptidoglycan synthesis creates a locally-acting, self-organizing mechanism allowing the rapid establishment and stable maintenance of emergent rod shape.

Article and author information

Author details

  1. Saman Hussain

    Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Carl N Wivagg

    Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Piotr Szwedziak

    MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5766-0873
  4. Felix Wong

    Harvard John A. Paulson School of Engineering and Applied Sciences, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2309-8835
  5. Kaitlin Schaefer

    Department of Microbiology and Immunology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Thierry Izoré

    MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Lars D Renner

    Leibniz Institute of Polymer Research, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Matthew J Holmes

    Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Yingjie Sun

    Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Alexandre W Bisson-Filho

    Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Suzanne Walker

    Department of Chemistry and Chemical Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Ariel Amir

    Harvard John A. Paulson School of Engineering and Applied Sciences, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2611-0139
  13. Jan Löwe

    MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5218-6615
  14. Ethan C Garner

    Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States
    For correspondence
    egarner@g.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0141-3555

Funding

National Institutes of Health (DP2AI117923-01)

  • Ethan C Garner

Volkswagen Foundation

  • Lars D Renner
  • Ariel Amir
  • Ethan C Garner

Wellcome (095514/Z/11/Z)

  • Jan Löwe

National Science Foundation (GFRP)

  • Felix Wong

Medical Research Council (U105184326)

  • Jan Löwe

Howard Hughes Medical Institute (International Student Research Fellow)

  • Saman Hussain

National Institutes of Health (R01 GM076710)

  • Suzanne Walker

Searle Scholar Fellowship

  • Ethan C Garner

Alfred P. Sloan Foundation

  • Ariel Amir

Smith Family Award

  • Ethan C Garner

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

Reviewing Editor

  1. Tâm Mignot, Aix Marseille University-CNRS UMR7283, France

Version history

  1. Received: October 3, 2017
  2. Accepted: February 21, 2018
  3. Accepted Manuscript published: February 22, 2018 (version 1)
  4. Accepted Manuscript updated: February 26, 2018 (version 2)
  5. Version of Record published: March 15, 2018 (version 3)

Copyright

© 2018, Hussain 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. Saman Hussain
  2. Carl N Wivagg
  3. Piotr Szwedziak
  4. Felix Wong
  5. Kaitlin Schaefer
  6. Thierry Izoré
  7. Lars D Renner
  8. Matthew J Holmes
  9. Yingjie Sun
  10. Alexandre W Bisson-Filho
  11. Suzanne Walker
  12. Ariel Amir
  13. Jan Löwe
  14. Ethan C Garner
(2018)
MreB filaments align along greatest principal membrane curvature to orient cell wall synthesis
eLife 7:e32471.
https://doi.org/10.7554/eLife.32471

Share this article

https://doi.org/10.7554/eLife.32471

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