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Cell envelope growth of Gram‐negative bacteria proceeds independently of cell wall synthesis

All bacterial cells must expand their envelopes during growth. The main load‐bearing and shape‐determining component of the bacterial envelope is the peptidoglycan cell wall. Bacterial envelope growth and shape changes are often thought to be controlled through enzymatic cell wall insertion. We inve...

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Autores principales: Oldewurtel, Enno R, Kitahara, Yuki, Cordier, Baptiste, Wheeler, Richard, Özbaykal, Gizem, Brambilla, Elisa, Boneca, Ivo Gomperts, Renner, Lars D, van Teeffelen, Sven
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10350831/
https://www.ncbi.nlm.nih.gov/pubmed/37260169
http://dx.doi.org/10.15252/embj.2022112168
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author Oldewurtel, Enno R
Kitahara, Yuki
Cordier, Baptiste
Wheeler, Richard
Özbaykal, Gizem
Brambilla, Elisa
Boneca, Ivo Gomperts
Renner, Lars D
van Teeffelen, Sven
author_facet Oldewurtel, Enno R
Kitahara, Yuki
Cordier, Baptiste
Wheeler, Richard
Özbaykal, Gizem
Brambilla, Elisa
Boneca, Ivo Gomperts
Renner, Lars D
van Teeffelen, Sven
author_sort Oldewurtel, Enno R
collection PubMed
description All bacterial cells must expand their envelopes during growth. The main load‐bearing and shape‐determining component of the bacterial envelope is the peptidoglycan cell wall. Bacterial envelope growth and shape changes are often thought to be controlled through enzymatic cell wall insertion. We investigated the role of cell wall insertion for cell shape changes during cell elongation in Gram‐negative bacteria. We found that both global and local rates of envelope growth of Escherichia coli remain nearly unperturbed upon arrest of cell wall insertion—up to the point of sudden cell lysis. Specifically, cells continue to expand their surface areas in proportion to biomass growth rate, even if the rate of mass growth changes. Other Gram‐negative bacteria behave similarly. Furthermore, cells plastically change cell shape in response to differential mechanical forces. Overall, we conclude that cell wall‐cleaving enzymes can control envelope growth independently of synthesis. Accordingly, the strong overexpression of an endopeptidase leads to transiently accelerated bacterial cell elongation. Our study demonstrates that biomass growth and envelope forces can guide cell envelope expansion through mechanisms that are independent of cell wall insertion.
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spelling pubmed-103508312023-07-18 Cell envelope growth of Gram‐negative bacteria proceeds independently of cell wall synthesis Oldewurtel, Enno R Kitahara, Yuki Cordier, Baptiste Wheeler, Richard Özbaykal, Gizem Brambilla, Elisa Boneca, Ivo Gomperts Renner, Lars D van Teeffelen, Sven EMBO J Articles All bacterial cells must expand their envelopes during growth. The main load‐bearing and shape‐determining component of the bacterial envelope is the peptidoglycan cell wall. Bacterial envelope growth and shape changes are often thought to be controlled through enzymatic cell wall insertion. We investigated the role of cell wall insertion for cell shape changes during cell elongation in Gram‐negative bacteria. We found that both global and local rates of envelope growth of Escherichia coli remain nearly unperturbed upon arrest of cell wall insertion—up to the point of sudden cell lysis. Specifically, cells continue to expand their surface areas in proportion to biomass growth rate, even if the rate of mass growth changes. Other Gram‐negative bacteria behave similarly. Furthermore, cells plastically change cell shape in response to differential mechanical forces. Overall, we conclude that cell wall‐cleaving enzymes can control envelope growth independently of synthesis. Accordingly, the strong overexpression of an endopeptidase leads to transiently accelerated bacterial cell elongation. Our study demonstrates that biomass growth and envelope forces can guide cell envelope expansion through mechanisms that are independent of cell wall insertion. John Wiley and Sons Inc. 2023-06-01 /pmc/articles/PMC10350831/ /pubmed/37260169 http://dx.doi.org/10.15252/embj.2022112168 Text en © 2023 The Authors. Published under the terms of the CC BY 4.0 license. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Articles
Oldewurtel, Enno R
Kitahara, Yuki
Cordier, Baptiste
Wheeler, Richard
Özbaykal, Gizem
Brambilla, Elisa
Boneca, Ivo Gomperts
Renner, Lars D
van Teeffelen, Sven
Cell envelope growth of Gram‐negative bacteria proceeds independently of cell wall synthesis
title Cell envelope growth of Gram‐negative bacteria proceeds independently of cell wall synthesis
title_full Cell envelope growth of Gram‐negative bacteria proceeds independently of cell wall synthesis
title_fullStr Cell envelope growth of Gram‐negative bacteria proceeds independently of cell wall synthesis
title_full_unstemmed Cell envelope growth of Gram‐negative bacteria proceeds independently of cell wall synthesis
title_short Cell envelope growth of Gram‐negative bacteria proceeds independently of cell wall synthesis
title_sort cell envelope growth of gram‐negative bacteria proceeds independently of cell wall synthesis
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10350831/
https://www.ncbi.nlm.nih.gov/pubmed/37260169
http://dx.doi.org/10.15252/embj.2022112168
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