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Membrane rigidity regulates E. coli proliferation rates

Combining single cell experiments, population dynamics and theoretical methods of membrane mechanics, we put forward that the rate of cell proliferation in E. coli colonies can be regulated by modifiers of the mechanical properties of the bacterial membrane. Bacterial proliferation was modelled as m...

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Autores principales: Salinas-Almaguer, Samuel, Mell, Michael, Almendro-Vedia, Victor G., Calero, Macarena, Robledo-Sánchez, Kevin Carlo Martín, Ruiz-Suarez, Carlos, Alarcón, Tomás, Barrio, Rafael A., Hernández-Machado, Aurora, Monroy, Francisco
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8766614/
https://www.ncbi.nlm.nih.gov/pubmed/35042922
http://dx.doi.org/10.1038/s41598-022-04970-0
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author Salinas-Almaguer, Samuel
Mell, Michael
Almendro-Vedia, Victor G.
Calero, Macarena
Robledo-Sánchez, Kevin Carlo Martín
Ruiz-Suarez, Carlos
Alarcón, Tomás
Barrio, Rafael A.
Hernández-Machado, Aurora
Monroy, Francisco
author_facet Salinas-Almaguer, Samuel
Mell, Michael
Almendro-Vedia, Victor G.
Calero, Macarena
Robledo-Sánchez, Kevin Carlo Martín
Ruiz-Suarez, Carlos
Alarcón, Tomás
Barrio, Rafael A.
Hernández-Machado, Aurora
Monroy, Francisco
author_sort Salinas-Almaguer, Samuel
collection PubMed
description Combining single cell experiments, population dynamics and theoretical methods of membrane mechanics, we put forward that the rate of cell proliferation in E. coli colonies can be regulated by modifiers of the mechanical properties of the bacterial membrane. Bacterial proliferation was modelled as mediated by cell division through a membrane constriction divisome based on FtsZ, a mechanically competent protein at elastic interaction against membrane rigidity. Using membrane fluctuation spectroscopy in the single cells, we revealed either membrane stiffening when considering hydrophobic long chain fatty substances, or membrane softening if short-chained hydrophilic molecules are used. Membrane stiffeners caused hindered growth under normal division in the microbial cultures, as expected for membrane rigidification. Membrane softeners, however, altered regular cell division causing persistent microbes that abnormally grow as long filamentous cells proliferating apparently faster. We invoke the concept of effective growth rate under the assumption of a heterogeneous population structure composed by distinguishable individuals with different FtsZ-content leading the possible forms of cell proliferation, from regular division in two normal daughters to continuous growing filamentation and budding. The results settle altogether into a master plot that captures a universal scaling between membrane rigidity and the divisional instability mediated by FtsZ at the onset of membrane constriction.
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spelling pubmed-87666142022-01-20 Membrane rigidity regulates E. coli proliferation rates Salinas-Almaguer, Samuel Mell, Michael Almendro-Vedia, Victor G. Calero, Macarena Robledo-Sánchez, Kevin Carlo Martín Ruiz-Suarez, Carlos Alarcón, Tomás Barrio, Rafael A. Hernández-Machado, Aurora Monroy, Francisco Sci Rep Article Combining single cell experiments, population dynamics and theoretical methods of membrane mechanics, we put forward that the rate of cell proliferation in E. coli colonies can be regulated by modifiers of the mechanical properties of the bacterial membrane. Bacterial proliferation was modelled as mediated by cell division through a membrane constriction divisome based on FtsZ, a mechanically competent protein at elastic interaction against membrane rigidity. Using membrane fluctuation spectroscopy in the single cells, we revealed either membrane stiffening when considering hydrophobic long chain fatty substances, or membrane softening if short-chained hydrophilic molecules are used. Membrane stiffeners caused hindered growth under normal division in the microbial cultures, as expected for membrane rigidification. Membrane softeners, however, altered regular cell division causing persistent microbes that abnormally grow as long filamentous cells proliferating apparently faster. We invoke the concept of effective growth rate under the assumption of a heterogeneous population structure composed by distinguishable individuals with different FtsZ-content leading the possible forms of cell proliferation, from regular division in two normal daughters to continuous growing filamentation and budding. The results settle altogether into a master plot that captures a universal scaling between membrane rigidity and the divisional instability mediated by FtsZ at the onset of membrane constriction. Nature Publishing Group UK 2022-01-18 /pmc/articles/PMC8766614/ /pubmed/35042922 http://dx.doi.org/10.1038/s41598-022-04970-0 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Salinas-Almaguer, Samuel
Mell, Michael
Almendro-Vedia, Victor G.
Calero, Macarena
Robledo-Sánchez, Kevin Carlo Martín
Ruiz-Suarez, Carlos
Alarcón, Tomás
Barrio, Rafael A.
Hernández-Machado, Aurora
Monroy, Francisco
Membrane rigidity regulates E. coli proliferation rates
title Membrane rigidity regulates E. coli proliferation rates
title_full Membrane rigidity regulates E. coli proliferation rates
title_fullStr Membrane rigidity regulates E. coli proliferation rates
title_full_unstemmed Membrane rigidity regulates E. coli proliferation rates
title_short Membrane rigidity regulates E. coli proliferation rates
title_sort membrane rigidity regulates e. coli proliferation rates
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8766614/
https://www.ncbi.nlm.nih.gov/pubmed/35042922
http://dx.doi.org/10.1038/s41598-022-04970-0
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