Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in Helicobacter pylori
- University of Washington, United States
- Princeton University, United States
- Fred Hutchinson Cancer Research Center, United States
- University of Delaware, United States
- Harvard Medical School, United States
- Newcastle University, United Kingdom
- 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.
Article and author information
Author details
Benjamin P Bratton
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
- Tâm Mignot, CNRS-Aix Marseille University, France
Version history
- Received: October 5, 2019
- Accepted: January 7, 2020
- Accepted Manuscript published: January 9, 2020 (version 1)
- 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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Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in Helicobacter pylori
eLife 9:e52482.
https://doi.org/10.7554/eLife.52482
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