Bacterial flagella grow through an injection-diffusion mechanism

  1. Thibaud T Renault
  2. Anthony O Abraham
  3. Tobias Bergmiller
  4. Guillaume Paradis
  5. Simon Rainville
  6. Emmanuelle Charpentier
  7. Călin C Guet
  8. Yuhai Tu
  9. Keiichi Namba
  10. James P Keener  Is a corresponding author
  11. Tohru Minamino
  12. Marc Erhardt  Is a corresponding author
  1. Helmholtz Centre for Infection Research, Germany
  2. Osaka University, Japan
  3. Institute of Science and Technology Austria, Austria
  4. Laval University, Canada
  5. Max Planck Institute for Infection Biology, Germany
  6. IBM Thomas J. Watson Research Center, United States
  7. University of Utah, United States

Abstract

The bacterial flagellum is a self-assembling nanomachine. The external flagellar filament, several times longer than a bacterial cell body, is made of a few tens of thousands subunits of a single protein: flagellin. A fundamental problem concerns the molecular mechanism of how the flagellum grows outside the cell, where no discernible energy source is available. Here, we monitored the dynamic assembly of individual flagella using in situ labelling and real-time immunostaining of elongating flagellar filaments. We report that the rate of flagellum growth, initially ∼1,700 amino acids per second, decreases with length and that the previously proposed chain mechanism does not contribute to the filament elongation dynamics. Inhibition of the proton motive force-dependent export apparatus revealed a major contribution of substrate injection in driving filament elongation. The combination of experimental and mathematical evidence demonstrates that a simple, injection-diffusion mechanism controls bacterial flagella growth outside the cell.

Article and author information

Author details

  1. Thibaud T Renault

    Junior Research Group Infection Biology of Salmonella, Helmholtz Centre for Infection Research, Braunschweig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Anthony O Abraham

    Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8710-1351
  3. Tobias Bergmiller

    Institute of Science and Technology Austria, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  4. Guillaume Paradis

    Department of Physics, Engineering Physics and Optics, Laval University, Quebec City, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Simon Rainville

    Department of Physics, Engineering Physics and Optics, Laval University, Quebec City, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Emmanuelle Charpentier

    Max Planck Institute for Infection Biology, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Călin C Guet

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6220-2052
  8. Yuhai Tu

    IBM Thomas J. Watson Research Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Keiichi Namba

    Graduate School of Frontier Biosciences, Osaka University, Suita, Japan
    Competing interests
    The authors declare that no competing interests exist.
  10. James P Keener

    Department of Mathematics, University of Utah, Salt Lake City, United States
    For correspondence
    keener@math.utah.edu
    Competing interests
    The authors declare that no competing interests exist.
  11. Tohru Minamino

    Graduate School of Frontier Biosciences, Osaka University, Suita, Japan
    Competing interests
    The authors declare that no competing interests exist.
  12. Marc Erhardt

    Junior Research Group Infection Biology of Salmonella, Helmholtz Centre for Infection Research, Braunschweig, Germany
    For correspondence
    marc.erhardt@helmholtz-hzi.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6292-619X

Funding

Helmholtz-Gemeinschaft (VH-NG-932)

  • Marc Erhardt

Japan Society for the Promotion of Science (15H01640)

  • Tohru Minamino

Max-Planck-Gesellschaft

  • Emmanuelle Charpentier

National Institutes of Health (R01GM081747)

  • Yuhai Tu

European Commission (334030)

  • Marc Erhardt

Japan Society for the Promotion of Science (25000013)

  • Keiichi Namba

Natural Sciences and Engineering Research Council of Canada

  • Simon Rainville

Alexander von Humboldt-Stiftung

  • Thibaud T Renault

Japan Society for the Promotion of Science (26293097)

  • Tohru Minamino

Japan Society for the Promotion of Science (24117004)

  • Tohru Minamino

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

Reviewing Editor

  1. Frank Jülicher, Max Planck Institute for the Physics of Complex Systems, Germany

Version history

  1. Received: November 11, 2016
  2. Accepted: March 4, 2017
  3. Accepted Manuscript published: March 6, 2017 (version 1)
  4. Version of Record published: April 10, 2017 (version 2)

Copyright

© 2017, Renault 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. Thibaud T Renault
  2. Anthony O Abraham
  3. Tobias Bergmiller
  4. Guillaume Paradis
  5. Simon Rainville
  6. Emmanuelle Charpentier
  7. Călin C Guet
  8. Yuhai Tu
  9. Keiichi Namba
  10. James P Keener
  11. Tohru Minamino
  12. Marc Erhardt
(2017)
Bacterial flagella grow through an injection-diffusion mechanism
eLife 6:e23136.
https://doi.org/10.7554/eLife.23136

Share this article

https://doi.org/10.7554/eLife.23136

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