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

doi:10.7554/eLife.52482

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

Research output: Contribution to journal › Article › peer-review

5 Scopus citations

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.

Original language	English (US)
Article number	e52482
Journal	eLife
Volume	9
DOIs	https://doi.org/10.7554/eLife.52482
State	Published - Jan 2020

All Science Journal Classification (ASJC) codes

Neuroscience(all)
Immunology and Microbiology(all)
Biochemistry, Genetics and Molecular Biology(all)

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10.7554/eLife.52482

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Taylor, J. A., Bratton, B. P., Sichel, S. R., Blair, K. M., Jacobs, H. M., Demeester, K. E., Kuru, E., Gray, J., Biboy, J., Vannieuwenhze, M. S., Vollmer, W., Grimes, C. L., Shaevitz, J. W., & Salama, N. R. (2020). Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in helicobacter pylori. eLife, 9, [e52482]. https://doi.org/10.7554/eLife.52482

Taylor, Jennifer A. ; Bratton, Benjamin P. ; Sichel, Sophie R. ; Blair, Kris M. ; Jacobs, Holly M. ; Demeester, Kristen E. ; Kuru, Erkin ; Gray, Joe ; Biboy, Jacob ; Vannieuwenhze, Michael S. ; Vollmer, Waldemar ; Grimes, Catherine L. ; Shaevitz, Joshua W. ; Salama, Nina R. / Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in helicobacter pylori. In: eLife. 2020 ; Vol. 9.

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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.",

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Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in helicobacter pylori. / Taylor, Jennifer A.; Bratton, Benjamin P.; Sichel, Sophie R.; Blair, Kris M.; Jacobs, Holly M.; Demeester, Kristen E.; Kuru, Erkin; Gray, Joe; Biboy, Jacob; Vannieuwenhze, Michael S.; Vollmer, Waldemar; Grimes, Catherine L.; Shaevitz, Joshua W.; Salama, Nina R.

In: eLife, Vol. 9, e52482, 01.2020.

Research output: Contribution to journal › Article › peer-review

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