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

Author:

Taylor Jennifer A12,Bratton Benjamin P34ORCID,Sichel Sophie R25,Blair Kris M26,Jacobs Holly M26,DeMeester Kristen E7,Kuru Erkin8,Gray Joe9ORCID,Biboy Jacob10ORCID,VanNieuwenhze Michael S11,Vollmer Waldemar10,Grimes Catherine L712,Shaevitz Joshua W313ORCID,Salama Nina R1256ORCID

Affiliation:

1. Department of Microbiology, University of Washington, Seattle, United States

2. Human Biology Division, Fred Hutchinson Cancer Research Center, Seattle, United States

3. Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, United States

4. Department of Molecular Biology, Princeton University, Princeton, United States

5. Molecular Medicine and Mechanisms of Disease Graduate Program, University of Washington, Seattle, United States

6. Molecular and Cellular Biology Graduate Program, University of Washington, Seattle, United States

7. Department of Chemistry and Biochemistry, University of Delaware, Newark, United States

8. Department of Genetics, Harvard Medical School, Boston, United States

9. Biosciences Institute, Newcastle University, Newcastle upon Tyne, United Kingdom

10. Centre for Bacterial Cell Biology, Biosciences Institute, Newcastle University, Newcastle upon Tyne, United Kingdom

11. Department of Chemistry, Indiana University, Bloomington, United States

12. Department of Biological Sciences, University of Delaware, Newark, United States

13. Department of Physics, Princeton University, Princeton, 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.

Funder

National Institutes of Health

National Center for Research Resources

Wellcome

National Science Foundation

Department of Defense

Graduate Opportunities and Minority Achievement Program

Glenn Centers for Aging Research

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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