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The Evolution of Quorum Sensing in Bacterial Biofilms
Bacteria have fascinating and diverse social lives. They display coordinated group behaviors regulated by quorum-sensing systems that detect the density of other bacteria around them. A key example of such group behavior is biofilm formation, in which communities of cells attach to a surface and env...
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Formato: | Texto |
Lenguaje: | English |
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Public Library of Science
2008
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2214811/ https://www.ncbi.nlm.nih.gov/pubmed/18232735 http://dx.doi.org/10.1371/journal.pbio.0060014 |
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author | Nadell, Carey D Xavier, Joao B Levin, Simon A Foster, Kevin R |
author_facet | Nadell, Carey D Xavier, Joao B Levin, Simon A Foster, Kevin R |
author_sort | Nadell, Carey D |
collection | PubMed |
description | Bacteria have fascinating and diverse social lives. They display coordinated group behaviors regulated by quorum-sensing systems that detect the density of other bacteria around them. A key example of such group behavior is biofilm formation, in which communities of cells attach to a surface and envelope themselves in secreted polymers. Curiously, after reaching high cell density, some bacterial species activate polymer secretion, whereas others terminate polymer secretion. Here, we investigate this striking variation in the first evolutionary model of quorum sensing in biofilms. We use detailed individual-based simulations to investigate evolutionary competitions between strains that differ in their polymer production and quorum-sensing phenotypes. The benefit of activating polymer secretion at high cell density is relatively straightforward: secretion starts upon biofilm formation, allowing strains to push their lineages into nutrient-rich areas and suffocate neighboring cells. But why use quorum sensing to terminate polymer secretion at high cell density? We find that deactivating polymer production in biofilms can yield an advantage by redirecting resources into growth, but that this advantage occurs only in a limited time window. We predict, therefore, that down-regulation of polymer secretion at high cell density will evolve when it can coincide with dispersal events, but it will be disfavored in long-lived (chronic) biofilms with sustained competition among strains. Our model suggests that the observed variation in quorum-sensing behavior can be linked to the differing requirements of bacteria in chronic versus acute biofilm infections. This is well illustrated by the case of Vibrio cholerae, which competes within biofilms by polymer secretion, terminates polymer secretion at high cell density, and induces an acute disease course that ends with mass dispersal from the host. More generally, this work shows that the balance of competition within and among biofilms can be pivotal in the evolution of quorum sensing. |
format | Text |
id | pubmed-2214811 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2008 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-22148112008-01-26 The Evolution of Quorum Sensing in Bacterial Biofilms Nadell, Carey D Xavier, Joao B Levin, Simon A Foster, Kevin R PLoS Biol Research Article Bacteria have fascinating and diverse social lives. They display coordinated group behaviors regulated by quorum-sensing systems that detect the density of other bacteria around them. A key example of such group behavior is biofilm formation, in which communities of cells attach to a surface and envelope themselves in secreted polymers. Curiously, after reaching high cell density, some bacterial species activate polymer secretion, whereas others terminate polymer secretion. Here, we investigate this striking variation in the first evolutionary model of quorum sensing in biofilms. We use detailed individual-based simulations to investigate evolutionary competitions between strains that differ in their polymer production and quorum-sensing phenotypes. The benefit of activating polymer secretion at high cell density is relatively straightforward: secretion starts upon biofilm formation, allowing strains to push their lineages into nutrient-rich areas and suffocate neighboring cells. But why use quorum sensing to terminate polymer secretion at high cell density? We find that deactivating polymer production in biofilms can yield an advantage by redirecting resources into growth, but that this advantage occurs only in a limited time window. We predict, therefore, that down-regulation of polymer secretion at high cell density will evolve when it can coincide with dispersal events, but it will be disfavored in long-lived (chronic) biofilms with sustained competition among strains. Our model suggests that the observed variation in quorum-sensing behavior can be linked to the differing requirements of bacteria in chronic versus acute biofilm infections. This is well illustrated by the case of Vibrio cholerae, which competes within biofilms by polymer secretion, terminates polymer secretion at high cell density, and induces an acute disease course that ends with mass dispersal from the host. More generally, this work shows that the balance of competition within and among biofilms can be pivotal in the evolution of quorum sensing. Public Library of Science 2008-01 2008-01-29 /pmc/articles/PMC2214811/ /pubmed/18232735 http://dx.doi.org/10.1371/journal.pbio.0060014 Text en © 2008 Nadell et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. |
spellingShingle | Research Article Nadell, Carey D Xavier, Joao B Levin, Simon A Foster, Kevin R The Evolution of Quorum Sensing in Bacterial Biofilms |
title | The Evolution of Quorum Sensing in Bacterial Biofilms |
title_full | The Evolution of Quorum Sensing in Bacterial Biofilms |
title_fullStr | The Evolution of Quorum Sensing in Bacterial Biofilms |
title_full_unstemmed | The Evolution of Quorum Sensing in Bacterial Biofilms |
title_short | The Evolution of Quorum Sensing in Bacterial Biofilms |
title_sort | evolution of quorum sensing in bacterial biofilms |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2214811/ https://www.ncbi.nlm.nih.gov/pubmed/18232735 http://dx.doi.org/10.1371/journal.pbio.0060014 |
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