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

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 neg...

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Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7012605/
https://www.ncbi.nlm.nih.gov/pubmed/31916938
http://dx.doi.org/10.7554/eLife.52482
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author 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
author_facet 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
author_sort Taylor, Jennifer A
collection PubMed
description 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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spelling pubmed-70126052020-02-12 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 eLife Microbiology and Infectious Disease 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. eLife Sciences Publications, Ltd 2020-01-09 /pmc/articles/PMC7012605/ /pubmed/31916938 http://dx.doi.org/10.7554/eLife.52482 Text en © 2020, Taylor et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Microbiology and Infectious Disease
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
title Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in Helicobacter pylori
title_full Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in Helicobacter pylori
title_fullStr Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in Helicobacter pylori
title_full_unstemmed Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in Helicobacter pylori
title_short Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in Helicobacter pylori
title_sort distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in helicobacter pylori
topic Microbiology and Infectious Disease
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7012605/
https://www.ncbi.nlm.nih.gov/pubmed/31916938
http://dx.doi.org/10.7554/eLife.52482
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