Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in Helicobacter pylori

  1. Jennifer A Taylor
  2. Benjamin P Bratton
  3. Sophie R Sichel
  4. Kris M Blair
  5. Holly M Jacobs
  6. Kristen E DeMeester
  7. Erkin Kuru
  8. Joe Gray
  9. Jacob Biboy
  10. Michael S VanNieuwenhze
  11. Waldemar Vollmer
  12. Catherine L Grimes
  13. Josh W Shaevitz
  14. Nina Reda Salama  Is a corresponding author
  1. University of Washington, United States
  2. Princeton University, United States
  3. Fred Hutchinson Cancer Research Center, United States
  4. University of Delaware, United States
  5. Harvard Medical School, United States
  6. Newcastle University, United Kingdom
  7. Indiana University, United States

Abstract

Helical cell shape is necessary for efficient stomach colonization by Helicobacter pylori, but the molecular mechanisms for generating helical shape remain unclear. The helical centerline pitch and radius of wild-type H. pylori cells dictate surface curvatures of considerably higher positive and negative Gaussian curvatures than those present in straight- or curved-rod H. pylori. Quantitative 3D microscopy analysis of short pulses with either N-acetylmuramic acid or D-alanine metabolic probes showed that cell wall growth is enhanced at both sidewall curvature extremes. Immunofluorescence revealed MreB is most abundant at negative Gaussian curvature, while the bactofilin CcmA is most abundant at positive Gaussian curvature. Strains expressing CcmA variants with altered polymerization properties lose helical shape and associated positive Gaussian curvatures. We thus propose a model where CcmA and MreB promote PG synthesis at positive and negative Gaussian curvatures, respectively, and that this patterning is one mechanism necessary for maintaining helical shape.

Data availability

The MATLAB scripts used to reconstruct cell surfaces and perform the geometric enrichment analyses are publicly available under a BSD 3-clause license at https://github.com/PrincetonUniversity/shae-cellshape-public and archived at https://doi.org/10.5281/zenodo.1248978.

The following previously published data sets were used

Article and author information

Author details

  1. Jennifer A Taylor

    Department of Microbiology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Benjamin P Bratton

    Lewis-Sigler Institute of Integrative Genomics, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1128-2560
  3. Sophie R Sichel

    Human Biology Division, Fred Hutchinson Cancer Research Center, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Kris M Blair

    Human Biology Division, Fred Hutchinson Cancer Research Center, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Holly M Jacobs

    Human Biology Division, Fred Hutchinson Cancer Research Center, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Kristen E DeMeester

    Department of Chemistry and Biochemistry, University of Delaware, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Erkin Kuru

    Department of Genetics, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Joe Gray

    Biosciences Institute, Newcastle University, Newcastle upon Tyne, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2338-0301
  9. Jacob Biboy

    Centre for Bacterial Cell Biology, Newcastle University, Newcastle upon Tyne, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1286-6851
  10. Michael S VanNieuwenhze

    Department of Chemistry, Indiana University, Bloomington, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Waldemar Vollmer

    Centre for Bacterial Cell Biology, Newcastle University, Newcastle upon Tyne, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  12. Catherine L Grimes

    Department of Chemistry and Biochemistry, University of Delaware, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Josh W Shaevitz

    Lewis-Sigler Institute of Integrative Genomics, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8809-4723
  14. Nina Reda Salama

    Human Biology Division, Fred Hutchinson Cancer Research Center, Seattle, United States
    For correspondence
    nsalama@fhcrc.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2762-1424

Funding

National Institutes of Health (R01 AI136946)

  • Nina Reda Salama

National Science Foundation (DGE-1256082)

  • Jennifer A Taylor
  • Kris M Blair

Department of Defense (National Defense Science & Engineering Graduate Fellowship (NDSEG))

  • Jennifer A Taylor

GO-MAP (Graduate Opportunity Program Research Assistantship Award)

  • Sophie R Sichel

National Science Foundation (PHY-1734030)

  • Benjamin P Bratton
  • Josh W Shaevitz

Glenn Centers for Aging Research

  • Benjamin P Bratton

National Institutes of Health (R21 AI121828)

  • Benjamin P Bratton
  • Josh W Shaevitz

National Institutes of Health (GM113172)

  • Michael S VanNieuwenhze

National Institutes of Health (U01 CA221230)

  • Catherine L Grimes
  • Nina Reda Salama

National Institutes of Health (T32 CA009657)

  • Kris M Blair

National Institutes of Health (T32 GM95421)

  • Sophie R Sichel

National Institutes of Health (T32 GM008550)

  • Kristen E DeMeester

National Institutes of Health (P30 CA015704)

  • Nina Reda Salama

National Center for Research Resources (Stanford Imaging Award Number 1S10OD01227601)

  • Nina Reda Salama

Wellcome (101824/Z/13/Z)

  • Waldemar Vollmer

National Science Foundation (DGE-0718124)

  • Jennifer A Taylor

The funders had no role in study design, datacollection and interpretation, or the decision to submit the work for publication. The opinions, findings, and conclusions or recommendationsexpressed in this material contents are solely the responsibility of the authors and do not necessarily represent the official views of the NCRR,the National Institutes of Health, the Department of Defense, or the National Science Foundation.

Reviewing Editor

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

Version history

  1. Received: October 5, 2019
  2. Accepted: January 7, 2020
  3. Accepted Manuscript published: January 9, 2020 (version 1)
  4. Version of Record published: February 11, 2020 (version 2)

Copyright

© 2020, Taylor 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. Jennifer A Taylor
  2. Benjamin P Bratton
  3. Sophie R Sichel
  4. Kris M Blair
  5. Holly M Jacobs
  6. Kristen E DeMeester
  7. Erkin Kuru
  8. Joe Gray
  9. Jacob Biboy
  10. Michael S VanNieuwenhze
  11. Waldemar Vollmer
  12. Catherine L Grimes
  13. Josh W Shaevitz
  14. Nina Reda Salama
(2020)
Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in Helicobacter pylori
eLife 9:e52482.
https://doi.org/10.7554/eLife.52482

Share this article

https://doi.org/10.7554/eLife.52482

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