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Nutrient complexity triggers transitions between solitary and colonial growth in bacterial populations

Microbial populations often experience fluctuations in nutrient complexity in their natural environment such as between high molecular weight polysaccharides and simple monosaccharides. However, it is unclear if cells can adopt growth behaviors that allow individuals to optimally respond to differen...

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Autores principales: D’Souza, Glen G., Povolo, Vanessa R., Keegstra, Johannes M., Stocker, Roman, Ackermann, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8397785/
https://www.ncbi.nlm.nih.gov/pubmed/33731836
http://dx.doi.org/10.1038/s41396-021-00953-7
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author D’Souza, Glen G.
Povolo, Vanessa R.
Keegstra, Johannes M.
Stocker, Roman
Ackermann, Martin
author_facet D’Souza, Glen G.
Povolo, Vanessa R.
Keegstra, Johannes M.
Stocker, Roman
Ackermann, Martin
author_sort D’Souza, Glen G.
collection PubMed
description Microbial populations often experience fluctuations in nutrient complexity in their natural environment such as between high molecular weight polysaccharides and simple monosaccharides. However, it is unclear if cells can adopt growth behaviors that allow individuals to optimally respond to differences in nutrient complexity. Here, we directly control nutrient complexity and use quantitative single-cell analysis to study the growth dynamics of individuals within populations of the aquatic bacterium Caulobacter crescentus. We show that cells form clonal microcolonies when growing on the polysaccharide xylan, which is abundant in nature and degraded using extracellular cell-linked enzymes; and disperse to solitary growth modes when the corresponding monosaccharide xylose becomes available or nutrients are exhausted. We find that the cellular density required to achieve maximal growth rates is four-fold higher on xylan than on xylose, indicating that aggregating is advantageous on polysaccharides. When collectives on xylan are transitioned to xylose, cells start dispersing, indicating that colony formation is no longer beneficial and solitary behaviors might serve to reduce intercellular competition. Our study demonstrates that cells can dynamically tune their behaviors when nutrient complexity fluctuates, elucidates the quantitative advantages of distinct growth behaviors for individual cells and indicates why collective growth modes are prevalent in microbial populations.
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spelling pubmed-83977852021-09-15 Nutrient complexity triggers transitions between solitary and colonial growth in bacterial populations D’Souza, Glen G. Povolo, Vanessa R. Keegstra, Johannes M. Stocker, Roman Ackermann, Martin ISME J Article Microbial populations often experience fluctuations in nutrient complexity in their natural environment such as between high molecular weight polysaccharides and simple monosaccharides. However, it is unclear if cells can adopt growth behaviors that allow individuals to optimally respond to differences in nutrient complexity. Here, we directly control nutrient complexity and use quantitative single-cell analysis to study the growth dynamics of individuals within populations of the aquatic bacterium Caulobacter crescentus. We show that cells form clonal microcolonies when growing on the polysaccharide xylan, which is abundant in nature and degraded using extracellular cell-linked enzymes; and disperse to solitary growth modes when the corresponding monosaccharide xylose becomes available or nutrients are exhausted. We find that the cellular density required to achieve maximal growth rates is four-fold higher on xylan than on xylose, indicating that aggregating is advantageous on polysaccharides. When collectives on xylan are transitioned to xylose, cells start dispersing, indicating that colony formation is no longer beneficial and solitary behaviors might serve to reduce intercellular competition. Our study demonstrates that cells can dynamically tune their behaviors when nutrient complexity fluctuates, elucidates the quantitative advantages of distinct growth behaviors for individual cells and indicates why collective growth modes are prevalent in microbial populations. Nature Publishing Group UK 2021-03-17 2021-09 /pmc/articles/PMC8397785/ /pubmed/33731836 http://dx.doi.org/10.1038/s41396-021-00953-7 Text en © The Author(s) 2021 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 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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
D’Souza, Glen G.
Povolo, Vanessa R.
Keegstra, Johannes M.
Stocker, Roman
Ackermann, Martin
Nutrient complexity triggers transitions between solitary and colonial growth in bacterial populations
title Nutrient complexity triggers transitions between solitary and colonial growth in bacterial populations
title_full Nutrient complexity triggers transitions between solitary and colonial growth in bacterial populations
title_fullStr Nutrient complexity triggers transitions between solitary and colonial growth in bacterial populations
title_full_unstemmed Nutrient complexity triggers transitions between solitary and colonial growth in bacterial populations
title_short Nutrient complexity triggers transitions between solitary and colonial growth in bacterial populations
title_sort nutrient complexity triggers transitions between solitary and colonial growth in bacterial populations
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8397785/
https://www.ncbi.nlm.nih.gov/pubmed/33731836
http://dx.doi.org/10.1038/s41396-021-00953-7
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