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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...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
John Wiley and Sons Inc.
2023
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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. |
format | Online Article Text |
id | pubmed-10350831 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | John Wiley and Sons Inc. |
record_format | MEDLINE/PubMed |
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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