Bacterial flagellar capping proteins adopt diverse oligomeric states

  1. Sandra Postel
  2. Daniel Deredge
  3. Daniel A Bonsor
  4. Xiong Yu
  5. Kay Diederichs
  6. Saskia Helmsing
  7. Aviv Vromen
  8. Assaf Friedler
  9. Michael Hust
  10. Edward H Egelman
  11. Dorothy Beckett
  12. Patrick L Wintrode
  13. Eric J Sundberg  Is a corresponding author
  1. University of Maryland School of Medicine, United States
  2. University of Maryland School of Pharmacy, United States
  3. University of Virginia, United States
  4. University of Konstanz, Germany
  5. Technische Universitaet Braunschweig, Germany
  6. The Hebrew University of Jerusalem, Israel
  7. Technische Universität Braunschweig, Germany
  8. University of Maryland College Park, United States

Abstract

Flagella are critical for bacterial motility and pathogenesis. The flagellar capping protein (FliD) regulates filament assembly by chaperoning and sorting flagellin (FliC) proteins after they traverse the hollow filament and exit the growing flagellum tip. In the absence of FliD, flagella are not formed resulting in impaired motility and infectivity. Here, we report the 2.2 Å resolution X-ray crystal structure of FliD from Pseudomonas aeruginosa, the first high-resolution structure of any FliD protein from any bacterium. In combination with a multitude of biophysical and functional analyses, we find that Pseudomonas FliD exhibits unexpected structural similarity to other flagellar proteins at the domain level, adopts a unique hexameric oligomeric state, and depends on flexible determinants for oligomerization. Considering that the flagellin filaments on which FliD oligomers are affixed vary between bacteria in protofilament number, our results suggest that FliD oligomer stoichiometries vary across bacteria to complement their filament assemblies.

Article and author information

Author details

  1. Sandra Postel

    Institute of Human Virology, University of Maryland School of Medicine, Baltimore, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6717-1870
  2. Daniel Deredge

    Department of Pharmaceutical Sciences, University of Maryland School of Pharmacy, Baltimore, United States
    Competing interests
    No competing interests declared.
  3. Daniel A Bonsor

    Institute of Human Virology, University of Maryland School of Medicine, Baltimore, United States
    Competing interests
    No competing interests declared.
  4. Xiong Yu

    Department of Biochemistry and Molecular Genetics, University of Virginia, Charlottesville, United States
    Competing interests
    No competing interests declared.
  5. Kay Diederichs

    Department of Biology, University of Konstanz, Konstanz, Germany
    Competing interests
    No competing interests declared.
  6. Saskia Helmsing

    Department of Biotechnology, Institute of Biochemistry, Biotechnology and Bioinformatics, Technische Universitaet Braunschweig, Braunschweig, Germany
    Competing interests
    No competing interests declared.
  7. Aviv Vromen

    Institute of Chemistry, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    No competing interests declared.
  8. Assaf Friedler

    Institute of Chemistry, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    No competing interests declared.
  9. Michael Hust

    Department of Biotechnology, Institute of Biochemistry, Biotechnology and Bioinformatics, Technische Universität Braunschweig, Braunschweig, Germany
    Competing interests
    No competing interests declared.
  10. Edward H Egelman

    Department of Biochemistry and Molecular Genetics, University of Virginia, Charlottesville, United States
    Competing interests
    Edward H Egelman, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4844-5212
  11. Dorothy Beckett

    Department of Chemistry and Biochemistry, University of Maryland College Park, Baltimore, United States
    Competing interests
    No competing interests declared.
  12. Patrick L Wintrode

    Department of Pharmaceutical Sciences, University of Maryland School of Pharmacy, Baltimore, United States
    Competing interests
    No competing interests declared.
  13. Eric J Sundberg

    Institute of Human Virology, University of Maryland School of Medicine, Baltimore, United States
    For correspondence
    ESundberg@ihv.umaryland.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0478-3033

Funding

National Center for Research Resources (NIH S10 RR15899)

  • Dorothy Beckett

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

Reviewing Editor

  1. Richard M Berry, University of Oxford, United Kingdom

Version history

  1. Received: June 15, 2016
  2. Accepted: September 23, 2016
  3. Accepted Manuscript published: September 24, 2016 (version 1)
  4. Version of Record published: October 20, 2016 (version 2)

Copyright

© 2016, Postel 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. Sandra Postel
  2. Daniel Deredge
  3. Daniel A Bonsor
  4. Xiong Yu
  5. Kay Diederichs
  6. Saskia Helmsing
  7. Aviv Vromen
  8. Assaf Friedler
  9. Michael Hust
  10. Edward H Egelman
  11. Dorothy Beckett
  12. Patrick L Wintrode
  13. Eric J Sundberg
(2016)
Bacterial flagellar capping proteins adopt diverse oligomeric states
eLife 5:e18857.
https://doi.org/10.7554/eLife.18857

Share this article

https://doi.org/10.7554/eLife.18857

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