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Evolution of Ecological Diversity in Biofilms of Pseudomonas aeruginosa by Altered Cyclic Diguanylate Signaling

The ecological and evolutionary forces that promote and maintain diversity in biofilms are not well understood. To quantify these forces, three Pseudomonas aeruginosa populations were experimentally evolved from strain PA14 in a daily cycle of attachment, assembly, and dispersal for 600 generations....

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Autores principales: Flynn, Kenneth M., Dowell, Gabrielle, Johnson, Thomas M., Koestler, Benjamin J., Waters, Christopher M., Cooper, Vaughn S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5019052/
https://www.ncbi.nlm.nih.gov/pubmed/27021563
http://dx.doi.org/10.1128/JB.00048-16
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author Flynn, Kenneth M.
Dowell, Gabrielle
Johnson, Thomas M.
Koestler, Benjamin J.
Waters, Christopher M.
Cooper, Vaughn S.
author_facet Flynn, Kenneth M.
Dowell, Gabrielle
Johnson, Thomas M.
Koestler, Benjamin J.
Waters, Christopher M.
Cooper, Vaughn S.
author_sort Flynn, Kenneth M.
collection PubMed
description The ecological and evolutionary forces that promote and maintain diversity in biofilms are not well understood. To quantify these forces, three Pseudomonas aeruginosa populations were experimentally evolved from strain PA14 in a daily cycle of attachment, assembly, and dispersal for 600 generations. Each biofilm population evolved diverse colony morphologies and mutator genotypes defective in DNA mismatch repair. This diversity enhanced population fitness and biofilm output, owing partly to rare, early colonizing mutants that enhanced attachment of others. Evolved mutants exhibited various levels of the intracellular signal cyclic-di-GMP, which associated with their timing of adherence. Manipulating cyclic-di-GMP levels within individual mutants revealed a network of interactions in the population that depended on various attachment strategies related to this signal. Diversification in biofilms may therefore arise and be reinforced by initial colonists that enable community assembly. IMPORTANCE How biofilm diversity assembles, evolves, and contributes to community function is largely unknown. This presents a major challenge for understanding evolution during chronic infections and during the growth of all surface-associated microbes. We used experimental evolution to probe these dynamics and found that diversity, partly related to altered cyclic-di-GMP levels, arose and persisted due to the emergence of ecological interdependencies related to attachment patterns. Clonal isolates failed to capture population attributes, which points to the need to account for diversity in infections. More broadly, this study offers an experimental framework for linking phenotypic variation to distinct ecological strategies in biofilms and for studying eco-evolutionary interactions.
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spelling pubmed-50190522016-09-23 Evolution of Ecological Diversity in Biofilms of Pseudomonas aeruginosa by Altered Cyclic Diguanylate Signaling Flynn, Kenneth M. Dowell, Gabrielle Johnson, Thomas M. Koestler, Benjamin J. Waters, Christopher M. Cooper, Vaughn S. J Bacteriol Meeting Presentations The ecological and evolutionary forces that promote and maintain diversity in biofilms are not well understood. To quantify these forces, three Pseudomonas aeruginosa populations were experimentally evolved from strain PA14 in a daily cycle of attachment, assembly, and dispersal for 600 generations. Each biofilm population evolved diverse colony morphologies and mutator genotypes defective in DNA mismatch repair. This diversity enhanced population fitness and biofilm output, owing partly to rare, early colonizing mutants that enhanced attachment of others. Evolved mutants exhibited various levels of the intracellular signal cyclic-di-GMP, which associated with their timing of adherence. Manipulating cyclic-di-GMP levels within individual mutants revealed a network of interactions in the population that depended on various attachment strategies related to this signal. Diversification in biofilms may therefore arise and be reinforced by initial colonists that enable community assembly. IMPORTANCE How biofilm diversity assembles, evolves, and contributes to community function is largely unknown. This presents a major challenge for understanding evolution during chronic infections and during the growth of all surface-associated microbes. We used experimental evolution to probe these dynamics and found that diversity, partly related to altered cyclic-di-GMP levels, arose and persisted due to the emergence of ecological interdependencies related to attachment patterns. Clonal isolates failed to capture population attributes, which points to the need to account for diversity in infections. More broadly, this study offers an experimental framework for linking phenotypic variation to distinct ecological strategies in biofilms and for studying eco-evolutionary interactions. American Society for Microbiology 2016-09-09 /pmc/articles/PMC5019052/ /pubmed/27021563 http://dx.doi.org/10.1128/JB.00048-16 Text en Copyright © 2016 Flynn et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Meeting Presentations
Flynn, Kenneth M.
Dowell, Gabrielle
Johnson, Thomas M.
Koestler, Benjamin J.
Waters, Christopher M.
Cooper, Vaughn S.
Evolution of Ecological Diversity in Biofilms of Pseudomonas aeruginosa by Altered Cyclic Diguanylate Signaling
title Evolution of Ecological Diversity in Biofilms of Pseudomonas aeruginosa by Altered Cyclic Diguanylate Signaling
title_full Evolution of Ecological Diversity in Biofilms of Pseudomonas aeruginosa by Altered Cyclic Diguanylate Signaling
title_fullStr Evolution of Ecological Diversity in Biofilms of Pseudomonas aeruginosa by Altered Cyclic Diguanylate Signaling
title_full_unstemmed Evolution of Ecological Diversity in Biofilms of Pseudomonas aeruginosa by Altered Cyclic Diguanylate Signaling
title_short Evolution of Ecological Diversity in Biofilms of Pseudomonas aeruginosa by Altered Cyclic Diguanylate Signaling
title_sort evolution of ecological diversity in biofilms of pseudomonas aeruginosa by altered cyclic diguanylate signaling
topic Meeting Presentations
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5019052/
https://www.ncbi.nlm.nih.gov/pubmed/27021563
http://dx.doi.org/10.1128/JB.00048-16
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