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Enforced specialization fosters mutual cheating and not division of labour in the bacterium Pseudomonas aeruginosa

A common way for bacteria to cooperate is via the secretion of beneficial public goods (proteases, siderophores, biosurfactants) that can be shared amongst individuals in a group. Bacteria often simultaneously deploy multiple public goods with complementary functions. This raises the question whethe...

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Autores principales: Mridha, Subham, Kümmerli, Rolf
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9323447/
https://www.ncbi.nlm.nih.gov/pubmed/35380743
http://dx.doi.org/10.1111/jeb.14001
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author Mridha, Subham
Kümmerli, Rolf
author_facet Mridha, Subham
Kümmerli, Rolf
author_sort Mridha, Subham
collection PubMed
description A common way for bacteria to cooperate is via the secretion of beneficial public goods (proteases, siderophores, biosurfactants) that can be shared amongst individuals in a group. Bacteria often simultaneously deploy multiple public goods with complementary functions. This raises the question whether natural selection could favour division of labour where subpopulations or species specialize in the production of a single public good, whilst sharing the complementary goods at the group level. Here we use an experimental system, where we mix engineered specialists of the bacterium Pseudomonas aeruginosa that can each only produce one of the two siderophores, pyochelin or pyoverdine and explore the conditions under which specialization can lead to division of labour. When growing pyochelin and pyoverdine specialists at different mixing ratios under different levels of iron limitation, we found that specialists could only successfully complement each other in environments with moderate iron limitation and grow as good as the generalist wildtype but not better. Under more stringent iron limitation, the dynamics in specialist communities was characterized by mutual cheating and with higher proportions of pyochelin producers greatly compromising group productivity. Nonetheless, specialist communities remained stable through negative frequency‐dependent selection. Our work shows that specialization in a bacterial community can be spurred by cheating and does not necessarily result in beneficial division of labour. We propose that natural selection might favour fine‐tuned regulatory mechanisms in generalists over division of labour because the former enables generalists to remain flexible and adequately adjust public good investments in fluctuating environments.
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spelling pubmed-93234472022-07-30 Enforced specialization fosters mutual cheating and not division of labour in the bacterium Pseudomonas aeruginosa Mridha, Subham Kümmerli, Rolf J Evol Biol Research Articles A common way for bacteria to cooperate is via the secretion of beneficial public goods (proteases, siderophores, biosurfactants) that can be shared amongst individuals in a group. Bacteria often simultaneously deploy multiple public goods with complementary functions. This raises the question whether natural selection could favour division of labour where subpopulations or species specialize in the production of a single public good, whilst sharing the complementary goods at the group level. Here we use an experimental system, where we mix engineered specialists of the bacterium Pseudomonas aeruginosa that can each only produce one of the two siderophores, pyochelin or pyoverdine and explore the conditions under which specialization can lead to division of labour. When growing pyochelin and pyoverdine specialists at different mixing ratios under different levels of iron limitation, we found that specialists could only successfully complement each other in environments with moderate iron limitation and grow as good as the generalist wildtype but not better. Under more stringent iron limitation, the dynamics in specialist communities was characterized by mutual cheating and with higher proportions of pyochelin producers greatly compromising group productivity. Nonetheless, specialist communities remained stable through negative frequency‐dependent selection. Our work shows that specialization in a bacterial community can be spurred by cheating and does not necessarily result in beneficial division of labour. We propose that natural selection might favour fine‐tuned regulatory mechanisms in generalists over division of labour because the former enables generalists to remain flexible and adequately adjust public good investments in fluctuating environments. John Wiley and Sons Inc. 2022-04-05 2022-05 /pmc/articles/PMC9323447/ /pubmed/35380743 http://dx.doi.org/10.1111/jeb.14001 Text en © 2022 The Authors. Journal of Evolutionary Biology published by John Wiley & Sons Ltd on behalf of European Society for Evolutionary Biology. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Research Articles
Mridha, Subham
Kümmerli, Rolf
Enforced specialization fosters mutual cheating and not division of labour in the bacterium Pseudomonas aeruginosa
title Enforced specialization fosters mutual cheating and not division of labour in the bacterium Pseudomonas aeruginosa
title_full Enforced specialization fosters mutual cheating and not division of labour in the bacterium Pseudomonas aeruginosa
title_fullStr Enforced specialization fosters mutual cheating and not division of labour in the bacterium Pseudomonas aeruginosa
title_full_unstemmed Enforced specialization fosters mutual cheating and not division of labour in the bacterium Pseudomonas aeruginosa
title_short Enforced specialization fosters mutual cheating and not division of labour in the bacterium Pseudomonas aeruginosa
title_sort enforced specialization fosters mutual cheating and not division of labour in the bacterium pseudomonas aeruginosa
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9323447/
https://www.ncbi.nlm.nih.gov/pubmed/35380743
http://dx.doi.org/10.1111/jeb.14001
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