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Nutrient limitation determines the fitness of cheaters in bacterial siderophore cooperation

Cooperative behaviors provide a collective benefit, but are considered costly for the individual. Here, we report that these costs vary dramatically in different contexts and have opposing effects on the selection for non-cooperating cheaters. We investigate a prominent example of bacterial cooperat...

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Autores principales: Sexton, D. Joseph, Schuster, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5550491/
https://www.ncbi.nlm.nih.gov/pubmed/28794499
http://dx.doi.org/10.1038/s41467-017-00222-2
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author Sexton, D. Joseph
Schuster, Martin
author_facet Sexton, D. Joseph
Schuster, Martin
author_sort Sexton, D. Joseph
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description Cooperative behaviors provide a collective benefit, but are considered costly for the individual. Here, we report that these costs vary dramatically in different contexts and have opposing effects on the selection for non-cooperating cheaters. We investigate a prominent example of bacterial cooperation, the secretion of the peptide siderophore pyoverdine by Pseudomonas aeruginosa, under different nutrient-limiting conditions. Using metabolic modeling, we show that pyoverdine incurs a fitness cost only when its building blocks carbon or nitrogen are growth-limiting and are diverted from cellular biomass production. We confirm this result experimentally with a continuous-culture approach. We show that pyoverdine non-producers (cheaters) enjoy a large fitness advantage in co-culture with producers (cooperators) and spread to high frequency when limited by carbon, but not when limited by phosphorus. The principle of nutrient-dependent fitness costs has implications for the stability of cooperation in pathogenic and non-pathogenic environments, in biotechnological applications, and beyond the microbial realm.
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spelling pubmed-55504912017-08-14 Nutrient limitation determines the fitness of cheaters in bacterial siderophore cooperation Sexton, D. Joseph Schuster, Martin Nat Commun Article Cooperative behaviors provide a collective benefit, but are considered costly for the individual. Here, we report that these costs vary dramatically in different contexts and have opposing effects on the selection for non-cooperating cheaters. We investigate a prominent example of bacterial cooperation, the secretion of the peptide siderophore pyoverdine by Pseudomonas aeruginosa, under different nutrient-limiting conditions. Using metabolic modeling, we show that pyoverdine incurs a fitness cost only when its building blocks carbon or nitrogen are growth-limiting and are diverted from cellular biomass production. We confirm this result experimentally with a continuous-culture approach. We show that pyoverdine non-producers (cheaters) enjoy a large fitness advantage in co-culture with producers (cooperators) and spread to high frequency when limited by carbon, but not when limited by phosphorus. The principle of nutrient-dependent fitness costs has implications for the stability of cooperation in pathogenic and non-pathogenic environments, in biotechnological applications, and beyond the microbial realm. Nature Publishing Group UK 2017-08-10 /pmc/articles/PMC5550491/ /pubmed/28794499 http://dx.doi.org/10.1038/s41467-017-00222-2 Text en © The Author(s) 2017 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
Sexton, D. Joseph
Schuster, Martin
Nutrient limitation determines the fitness of cheaters in bacterial siderophore cooperation
title Nutrient limitation determines the fitness of cheaters in bacterial siderophore cooperation
title_full Nutrient limitation determines the fitness of cheaters in bacterial siderophore cooperation
title_fullStr Nutrient limitation determines the fitness of cheaters in bacterial siderophore cooperation
title_full_unstemmed Nutrient limitation determines the fitness of cheaters in bacterial siderophore cooperation
title_short Nutrient limitation determines the fitness of cheaters in bacterial siderophore cooperation
title_sort nutrient limitation determines the fitness of cheaters in bacterial siderophore cooperation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5550491/
https://www.ncbi.nlm.nih.gov/pubmed/28794499
http://dx.doi.org/10.1038/s41467-017-00222-2
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