1. Microbiology and Infectious Disease
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Cyclic di-GMP differentially tunes a bacterial flagellar motor through a novel class of CheY-like regulators

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Cite this article as: eLife 2017;6:e28842 doi: 10.7554/eLife.28842

Abstract

The flagellar motor is a sophisticated rotary machine facilitating locomotion and signal transduction. Owing to its important role in bacterial behavior, its assembly and activity are tightly regulated. For example, chemotaxis relies on a sensory pathway coupling chemical information to rotational bias of the motor through phosphorylation of the motor switch protein CheY. Using a chemical proteomics approach, we identified a novel family of CheY-like (Cle) proteins in Caulobacter crescentus, which tune flagellar activity in response to binding of the second messenger c-di-GMP to a C-terminal extension. In their c-di-GMP bound conformation Cle proteins interact with the flagellar switch to control motor activity. We show that individual Cle proteins have adopted discrete cellular functions by interfering with chemotaxis and by promoting rapid surface attachment of motile cells. This study broadens the regulatory versatility of bacterial motors and unfolds mechanisms that tie motor activity to mechanical cues and bacterial surface adaptation.

Article and author information

Author details

  1. Jutta Nesper

    Focal Area of Infection Biology, Biozentrum, University of Basel, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Isabelle Hug

    Focal Area of Infection Biology, Biozentrum, University of Basel, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Setsu Kato

    Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Chee-Seng Hee

    Focal Area of Structural Biology and Biophysics, Biozentrum, University of Basel, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Judith Maria Habazettl

    Focal Area of Structural Biology and Biophysics, Biozentrum, University of Basel, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  6. Pablo Manfredi

    Focal Area of Infection Biology, Biozentrum, University of Basel, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  7. Stephan Grzesiek

    Focal Area of Structural Biology and Biophysics, Biozentrum, University of Basel, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  8. Tilman Schirmer

    Focal Area of Structural Biology and Biophysics, Biozentrum, University of Basel, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  9. Thierry Emonet

    Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6746-6564
  10. Urs Jenal

    Focal Area of Infection Biology, Biozentrum, University of Basel, Basel, Switzerland
    For correspondence
    urs.jenal@unibas.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1637-3376

Funding

European Research Council (Advanced Research Grant to U.J.)

  • Urs Jenal

Paul G. Allen Family Foundation (award no. 11562)

  • Thierry Emonet

Swiss National Science Foundation (Sinergia grant CRSII3_127433)

  • Urs Jenal

National Institutes of Health (grant no. 1R01GM106189)

  • Thierry Emonet

Swiss National Science Foundation (grant 31003A_166652)

  • Tilman Schirmer

Swiss National Science Foundation (grant 31003A_173089)

  • Stephan Grzesiek

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

Publication history

  1. Received: May 19, 2017
  2. Accepted: October 28, 2017
  3. Accepted Manuscript published: November 1, 2017 (version 1)
  4. Version of Record published: November 8, 2017 (version 2)

Copyright

© 2017, Nesper 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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