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Multicellular behaviour enables cooperation in microbial cell aggregates

Oligosaccharides produced from the extracellular hydrolysis of biological materials can act as common goods that promote cooperative growth in microbial populations, whereby cell–cell aggregation increases both the per capita availability of resources and the per-cell growth rate. However, aggregati...

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Detalles Bibliográficos
Autores principales: Ebrahimi, Ali, Schwartzman, Julia, Cordero, Otto X.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6792450/
https://www.ncbi.nlm.nih.gov/pubmed/31587643
http://dx.doi.org/10.1098/rstb.2019.0077
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author Ebrahimi, Ali
Schwartzman, Julia
Cordero, Otto X.
author_facet Ebrahimi, Ali
Schwartzman, Julia
Cordero, Otto X.
author_sort Ebrahimi, Ali
collection PubMed
description Oligosaccharides produced from the extracellular hydrolysis of biological materials can act as common goods that promote cooperative growth in microbial populations, whereby cell–cell aggregation increases both the per capita availability of resources and the per-cell growth rate. However, aggregation can also have detrimental consequences for growth, as gradients form within aggregates limiting the resource accessibility. We built a computational model, which predicts cooperation is restricted in dense cell aggregates larger than 10 µm because of the emergence of polymer and oligomer counter gradients. We compared these predictions to experiments performed with two well-studied alginate-degrading strains of Vibrio splendidus, which varied in their ability to secrete alginate lyase. We observed that both strains can form large aggregates (less than 50 µm), overcoming diffusion limitation by rearranging their internal structure. The stronger enzyme producer grew non-cooperatively and formed aggregates with internal channels that allowed exchange between the bulk environment and the aggregate, whereas the weak enzyme producer showed strongly cooperative growth and formed dense aggregates in which cells near the core mixed by active swimming. Our simulations suggest that the mixing and channelling reduce diffusion limitation and allow cells to uniformly grow in aggregates. Together, these data demonstrate that bacterial behaviour can help overcome competition imposed by resource gradients within cell aggregates. This article is part of a discussion meeting issue ‘Single cell ecology’.
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spelling pubmed-67924502019-10-19 Multicellular behaviour enables cooperation in microbial cell aggregates Ebrahimi, Ali Schwartzman, Julia Cordero, Otto X. Philos Trans R Soc Lond B Biol Sci Articles Oligosaccharides produced from the extracellular hydrolysis of biological materials can act as common goods that promote cooperative growth in microbial populations, whereby cell–cell aggregation increases both the per capita availability of resources and the per-cell growth rate. However, aggregation can also have detrimental consequences for growth, as gradients form within aggregates limiting the resource accessibility. We built a computational model, which predicts cooperation is restricted in dense cell aggregates larger than 10 µm because of the emergence of polymer and oligomer counter gradients. We compared these predictions to experiments performed with two well-studied alginate-degrading strains of Vibrio splendidus, which varied in their ability to secrete alginate lyase. We observed that both strains can form large aggregates (less than 50 µm), overcoming diffusion limitation by rearranging their internal structure. The stronger enzyme producer grew non-cooperatively and formed aggregates with internal channels that allowed exchange between the bulk environment and the aggregate, whereas the weak enzyme producer showed strongly cooperative growth and formed dense aggregates in which cells near the core mixed by active swimming. Our simulations suggest that the mixing and channelling reduce diffusion limitation and allow cells to uniformly grow in aggregates. Together, these data demonstrate that bacterial behaviour can help overcome competition imposed by resource gradients within cell aggregates. This article is part of a discussion meeting issue ‘Single cell ecology’. The Royal Society 2019-11-25 2019-10-07 /pmc/articles/PMC6792450/ /pubmed/31587643 http://dx.doi.org/10.1098/rstb.2019.0077 Text en © 2019 The Authors. http://creativecommons.org/licenses/by/4.0/ Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Articles
Ebrahimi, Ali
Schwartzman, Julia
Cordero, Otto X.
Multicellular behaviour enables cooperation in microbial cell aggregates
title Multicellular behaviour enables cooperation in microbial cell aggregates
title_full Multicellular behaviour enables cooperation in microbial cell aggregates
title_fullStr Multicellular behaviour enables cooperation in microbial cell aggregates
title_full_unstemmed Multicellular behaviour enables cooperation in microbial cell aggregates
title_short Multicellular behaviour enables cooperation in microbial cell aggregates
title_sort multicellular behaviour enables cooperation in microbial cell aggregates
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6792450/
https://www.ncbi.nlm.nih.gov/pubmed/31587643
http://dx.doi.org/10.1098/rstb.2019.0077
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