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Architecture and assembly of the Gram-positive cell wall

Beeby, Morgan and Gumbart, James C. and Roux, Benoît and Jensen, Grant J. (2013) Architecture and assembly of the Gram-positive cell wall. Molecular Microbiology, 88 (4). pp. 664-672. ISSN 0950-382X. PMCID PMC3663049. doi:10.1111/mmi.12203. https://resolver.caltech.edu/CaltechAUTHORS:20130624-103414394

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Abstract

The bacterial cell wall is a mesh polymer of peptidoglycan – linear glycan strands cross-linked by flexible peptides – that determines cell shape and provides physical protection. While the glycan strands in thin ‘Gram-negative’ peptidoglycan are known to run circumferentially around the cell, the architecture of the thicker ‘Gram-positive’ form remains unclear. Using electron cryotomography, here we show that Bacillus subtilis peptidoglycan is a uniformly dense layer with a textured surface. We further show it rips circumferentially, curls and thickens at free edges, and extends longitudinally when denatured. Molecular dynamics simulations show that only atomic models based on the circumferential topology recapitulate the observed curling and thickening, in support of an ‘inside-to-outside’ assembly process. We conclude that instead of being perpendicular to the cell surface or wrapped in coiled cables (two alternative models), the glycan strands in Gram-positive cell walls run circumferentially around the cell just as they do in Gram-negative cells. Together with providing insights into the architecture of the ultimate determinant of cell shape, this study is important because Gram-positive peptidoglycan is an antibiotic target crucial to the viability of several important rod-shaped pathogens including Bacillus anthracis, Listeria monocytogenes, and Clostridium difficile.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://onlinelibrary.wiley.com/doi/10.1111/mmi.12203/abstractPublisherArticle
http://dx.doi.org/doi:10.1111/mmi.12203DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3663049/PubMed CentralArticle
ORCID:
AuthorORCID
Beeby, Morgan0000-0001-6413-9835
Jensen, Grant J.0000-0003-1556-4864
Additional Information:© 2013 John Wiley & Sons Ltd. Accepted 4 March, 2013. Article first published online: 22 Apr. 2013. We would like to thank Simon Foster for an initial gift of purified B. subtilis sacculi and the laboratory of Doug Rees for use of the MPBio FastPrep-24. This work was funded by National Institute of Health Grant R01 GM062342 to B. R., an Argonne Director’s Postdoctoral Fellowship (J. C. G.), the Howard Hughes Medical Institute, and the Gordon and Betty Moore Center for Integrative Study of Cell Regulation at Caltech. Simulations were carried out with resources provided by the Computation Institute and the Biological Sciences Division of the University of Chicago and Argonne National Laboratory, under Grant S10 RR029030-01. We would also like to thank Brigitte Ziervogel for helpful comments on the manuscript.
Funders:
Funding AgencyGrant Number
NIHR01 GM062342
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Gordon and Betty Moore FoundationUNSPECIFIED
Argonne National LaboratoryS10 RR029030-01
Issue or Number:4
PubMed Central ID:PMC3663049
DOI:10.1111/mmi.12203
Record Number:CaltechAUTHORS:20130624-103414394
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20130624-103414394
Official Citation:Beeby, M., Gumbart, J. C., Roux, B. and Jensen, G. J. (2013), Architecture and assembly of the Gram-positive cell wall. Molecular Microbiology, 88: 664–672. doi: 10.1111/mmi.12203
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:39049
Collection:CaltechAUTHORS
Deposited By: John Wade
Deposited On:24 Jun 2013 18:24
Last Modified:09 Nov 2021 23:42

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