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Precise regulation of the relative rates of surface area and volume synthesis in bacterial cells growing in dynamic environments

The steady-state size of bacterial cells correlates with nutrient-determined growth rate. Here, we explore how rod-shaped bacterial cells regulate their morphology during rapid environmental changes. We quantify cellular dimensions throughout passage cycles of stationary-phase cells diluted into fre...

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Autores principales: Shi, Handuo, Hu, Yan, Odermatt, Pascal D., Gonzalez, Carlos G., Zhang, Lichao, Elias, Joshua E., Chang, Fred, Huang, Kerwyn Casey
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8009875/
https://www.ncbi.nlm.nih.gov/pubmed/33785742
http://dx.doi.org/10.1038/s41467-021-22092-5
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author Shi, Handuo
Hu, Yan
Odermatt, Pascal D.
Gonzalez, Carlos G.
Zhang, Lichao
Elias, Joshua E.
Chang, Fred
Huang, Kerwyn Casey
author_facet Shi, Handuo
Hu, Yan
Odermatt, Pascal D.
Gonzalez, Carlos G.
Zhang, Lichao
Elias, Joshua E.
Chang, Fred
Huang, Kerwyn Casey
author_sort Shi, Handuo
collection PubMed
description The steady-state size of bacterial cells correlates with nutrient-determined growth rate. Here, we explore how rod-shaped bacterial cells regulate their morphology during rapid environmental changes. We quantify cellular dimensions throughout passage cycles of stationary-phase cells diluted into fresh medium and grown back to saturation. We find that cells exhibit characteristic dynamics in surface area to volume ratio (SA/V), which are conserved across genetic and chemical perturbations as well as across species and growth temperatures. A mathematical model with a single fitting parameter (the time delay between surface and volume synthesis) is quantitatively consistent with our SA/V experimental observations. The model supports that this time delay is due to differential expression of volume and surface-related genes, and that the first division after dilution occurs at a tightly controlled SA/V. Our minimal model thus provides insight into the connections between bacterial growth rate and cell shape in dynamic environments.
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spelling pubmed-80098752021-04-16 Precise regulation of the relative rates of surface area and volume synthesis in bacterial cells growing in dynamic environments Shi, Handuo Hu, Yan Odermatt, Pascal D. Gonzalez, Carlos G. Zhang, Lichao Elias, Joshua E. Chang, Fred Huang, Kerwyn Casey Nat Commun Article The steady-state size of bacterial cells correlates with nutrient-determined growth rate. Here, we explore how rod-shaped bacterial cells regulate their morphology during rapid environmental changes. We quantify cellular dimensions throughout passage cycles of stationary-phase cells diluted into fresh medium and grown back to saturation. We find that cells exhibit characteristic dynamics in surface area to volume ratio (SA/V), which are conserved across genetic and chemical perturbations as well as across species and growth temperatures. A mathematical model with a single fitting parameter (the time delay between surface and volume synthesis) is quantitatively consistent with our SA/V experimental observations. The model supports that this time delay is due to differential expression of volume and surface-related genes, and that the first division after dilution occurs at a tightly controlled SA/V. Our minimal model thus provides insight into the connections between bacterial growth rate and cell shape in dynamic environments. Nature Publishing Group UK 2021-03-30 /pmc/articles/PMC8009875/ /pubmed/33785742 http://dx.doi.org/10.1038/s41467-021-22092-5 Text en © The Author(s) 2021 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Shi, Handuo
Hu, Yan
Odermatt, Pascal D.
Gonzalez, Carlos G.
Zhang, Lichao
Elias, Joshua E.
Chang, Fred
Huang, Kerwyn Casey
Precise regulation of the relative rates of surface area and volume synthesis in bacterial cells growing in dynamic environments
title Precise regulation of the relative rates of surface area and volume synthesis in bacterial cells growing in dynamic environments
title_full Precise regulation of the relative rates of surface area and volume synthesis in bacterial cells growing in dynamic environments
title_fullStr Precise regulation of the relative rates of surface area and volume synthesis in bacterial cells growing in dynamic environments
title_full_unstemmed Precise regulation of the relative rates of surface area and volume synthesis in bacterial cells growing in dynamic environments
title_short Precise regulation of the relative rates of surface area and volume synthesis in bacterial cells growing in dynamic environments
title_sort precise regulation of the relative rates of surface area and volume synthesis in bacterial cells growing in dynamic environments
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8009875/
https://www.ncbi.nlm.nih.gov/pubmed/33785742
http://dx.doi.org/10.1038/s41467-021-22092-5
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