The presence and absence of periplasmic rings in bacterial flagellar motors correlates with stator type

  1. Mohammed Kaplan
  2. Debnath Ghosal
  3. Poorna Subramanian
  4. Catherine M Oikonomou
  5. Andreas Kjaer
  6. Sahand Pirbadian
  7. Davi R Ortega
  8. Ariane Briegel
  9. Mohamed Y El-Naggar
  10. Grant J Jensen  Is a corresponding author
  1. California Institute of Technology, United States
  2. University of Southern California, United States

Abstract

The bacterial flagellar motor, a cell-envelope-embedded macromolecular machine that functions as a cellular propeller, exhibits significant structural variability between species. Different torque-generating stator modules allow motors to operate in different pH, salt or viscosity levels. How such diversity evolved is unknown. Here we use electron cryo-tomography to determine the in situ macromolecular structures of three Gammaproteobacteria motors: Legionella pneumophila, Pseudomonas aeruginosa, and Shewanella oneidensis, providing the first views of intact motors with dual stator systems. Complementing our imaging with bioinformatics analysis, we find a correlation between the motor's stator system and its structural elaboration. Motors with a single H+-driven stator have only the core periplasmic P- and L-rings; those with dual H+-driven stators have an elaborated P-ring; and motors with Na+ or Na+/H+-driven stators have both their P- and L-rings embellished. Our results suggest an evolution of structural elaboration that may have enabled pathogenic bacteria to colonize higher-viscosity environments in animal hosts.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.The ECT structures have been deposited in the EMDB under the following accession numbers, EMD-0464 for Legionella pneumophila motor, EMD-0465 for Pseudomonas aeruginosa motor and EMD-0467 for Shewanella oneidensis MR-1 motor

The following data sets were generated

Article and author information

Author details

  1. Mohammed Kaplan

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Debnath Ghosal

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Poorna Subramanian

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Catherine M Oikonomou

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Andreas Kjaer

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0096-5764
  6. Sahand Pirbadian

    Department of Physics, Biological Sciences and Chemistry, University of Southern California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Davi R Ortega

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Ariane Briegel

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3733-3725
  9. Mohamed Y El-Naggar

    Department of Physics and Astronomy, Biological Sciences, and Chemistry, University of Southern California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Grant J Jensen

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    For correspondence
    jensen@caltech.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1556-4864

Funding

National Institutes of Health (R01 AI127401)

  • Mohammed Kaplan
  • Debnath Ghosal
  • Poorna Subramanian
  • Catherine M Oikonomou
  • Andreas Kjaer
  • Davi R Ortega
  • Ariane Briegel
  • Grant J Jensen

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (Rubicon fellowship)

  • Mohammed Kaplan

Air Force Office of Scientific Research

  • Sahand Pirbadian

Air Force Office of Scientific Research (FA955014-1-0294)

  • Mohamed Y El-Naggar

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

Reviewing Editor

  1. Edward H Egelman, University of Virginia, United States

Publication history

  1. Received: November 8, 2018
  2. Accepted: December 19, 2018
  3. Accepted Manuscript published: January 16, 2019 (version 1)
  4. Version of Record published: February 14, 2019 (version 2)

Copyright

© 2019, Kaplan 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. Mohammed Kaplan
  2. Debnath Ghosal
  3. Poorna Subramanian
  4. Catherine M Oikonomou
  5. Andreas Kjaer
  6. Sahand Pirbadian
  7. Davi R Ortega
  8. Ariane Briegel
  9. Mohamed Y El-Naggar
  10. Grant J Jensen
(2019)
The presence and absence of periplasmic rings in bacterial flagellar motors correlates with stator type
eLife 8:e43487.
https://doi.org/10.7554/eLife.43487

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