Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in Helicobacter pylori
Jennifer A Taylor,
Benjamin P Bratton,
Sophie R Sichel,
Kris M Blair,
Holly M Jacobs,
Kristen E DeMeester,
Erkin Kuru,
Joe Gray,
Jacob Biboy,
Michael S VanNieuwenhze,
Waldemar Vollmer,
Catherine L Grimes,
Joshua W Shaevitz,
Nina R Salama
Affiliations
Jennifer A Taylor
Department of Microbiology, University of Washington, Seattle, United States; Human Biology Division, Fred Hutchinson Cancer Research Center, Seattle, United States
Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, United States; Department of Molecular Biology, Princeton University, Princeton, United States
Sophie R Sichel
Human Biology Division, Fred Hutchinson Cancer Research Center, Seattle, United States; Molecular Medicine and Mechanisms of Disease Graduate Program, University of Washington, Seattle, United States
Kris M Blair
Human Biology Division, Fred Hutchinson Cancer Research Center, Seattle, United States; Molecular and Cellular Biology Graduate Program, University of Washington, Seattle, United States
Holly M Jacobs
Human Biology Division, Fred Hutchinson Cancer Research Center, Seattle, United States; Molecular and Cellular Biology Graduate Program, University of Washington, Seattle, United States
Kristen E DeMeester
Department of Chemistry and Biochemistry, University of Delaware, Newark, United States
Erkin Kuru
Department of Genetics, Harvard Medical School, Boston, United States
Centre for Bacterial Cell Biology, Biosciences Institute, Newcastle University, Newcastle upon Tyne, United Kingdom
Michael S VanNieuwenhze
Department of Chemistry, Indiana University, Bloomington, United States
Waldemar Vollmer
Centre for Bacterial Cell Biology, Biosciences Institute, Newcastle University, Newcastle upon Tyne, United Kingdom
Catherine L Grimes
Department of Chemistry and Biochemistry, University of Delaware, Newark, United States; Department of Biological Sciences, University of Delaware, Newark, United States
Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, United States; Department of Physics, Princeton University, Princeton, United States
Department of Microbiology, University of Washington, Seattle, United States; Human Biology Division, Fred Hutchinson Cancer Research Center, Seattle, United States; Molecular Medicine and Mechanisms of Disease Graduate Program, University of Washington, Seattle, United States; Molecular and Cellular Biology Graduate Program, University of Washington, Seattle, United States
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.
