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Cheaters shape the evolution of phenotypic heterogeneity in Bacillus subtilis biofilms

Biofilms are closely packed cells held and shielded by extracellular matrix composed of structural proteins and exopolysaccharides (EPS). As matrix components are costly to produce and shared within the population, EPS-deficient cells can act as cheaters by gaining benefits from the cooperative natu...

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Autores principales: Martin, Marivic, Dragoš, Anna, Otto, Simon B., Schäfer, Daniel, Brix, Susanne, Maróti, Gergely, Kovács, Ákos T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7608354/
https://www.ncbi.nlm.nih.gov/pubmed/32483306
http://dx.doi.org/10.1038/s41396-020-0685-4
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author Martin, Marivic
Dragoš, Anna
Otto, Simon B.
Schäfer, Daniel
Brix, Susanne
Maróti, Gergely
Kovács, Ákos T.
author_facet Martin, Marivic
Dragoš, Anna
Otto, Simon B.
Schäfer, Daniel
Brix, Susanne
Maróti, Gergely
Kovács, Ákos T.
author_sort Martin, Marivic
collection PubMed
description Biofilms are closely packed cells held and shielded by extracellular matrix composed of structural proteins and exopolysaccharides (EPS). As matrix components are costly to produce and shared within the population, EPS-deficient cells can act as cheaters by gaining benefits from the cooperative nature of EPS producers. Remarkably, genetically programmed EPS producers can also exhibit phenotypic heterogeneity at single-cell level. Previous studies have shown that spatial structure of biofilms limits the spread of cheaters, but the long-term influence of cheating on biofilm evolution is not well understood. Here, we examine the influence of EPS nonproducers on evolution of matrix production within the populations of EPS producers in a model biofilm-forming bacterium, Bacillus subtilis. We discovered that general adaptation to biofilm lifestyle leads to an increase in phenotypical heterogeneity of eps expression. However, prolonged exposure to EPS-deficient cheaters may result in different adaptive strategy, where eps expression increases uniformly within the population. We propose a molecular mechanism behind such adaptive strategy and demonstrate how it can benefit the EPS producers in the presence of cheaters. This study provides additional insights on how biofilms adapt and respond to stress caused by exploitation in long-term scenario.
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spelling pubmed-76083542020-11-05 Cheaters shape the evolution of phenotypic heterogeneity in Bacillus subtilis biofilms Martin, Marivic Dragoš, Anna Otto, Simon B. Schäfer, Daniel Brix, Susanne Maróti, Gergely Kovács, Ákos T. ISME J Article Biofilms are closely packed cells held and shielded by extracellular matrix composed of structural proteins and exopolysaccharides (EPS). As matrix components are costly to produce and shared within the population, EPS-deficient cells can act as cheaters by gaining benefits from the cooperative nature of EPS producers. Remarkably, genetically programmed EPS producers can also exhibit phenotypic heterogeneity at single-cell level. Previous studies have shown that spatial structure of biofilms limits the spread of cheaters, but the long-term influence of cheating on biofilm evolution is not well understood. Here, we examine the influence of EPS nonproducers on evolution of matrix production within the populations of EPS producers in a model biofilm-forming bacterium, Bacillus subtilis. We discovered that general adaptation to biofilm lifestyle leads to an increase in phenotypical heterogeneity of eps expression. However, prolonged exposure to EPS-deficient cheaters may result in different adaptive strategy, where eps expression increases uniformly within the population. We propose a molecular mechanism behind such adaptive strategy and demonstrate how it can benefit the EPS producers in the presence of cheaters. This study provides additional insights on how biofilms adapt and respond to stress caused by exploitation in long-term scenario. Nature Publishing Group UK 2020-06-01 2020-09 /pmc/articles/PMC7608354/ /pubmed/32483306 http://dx.doi.org/10.1038/s41396-020-0685-4 Text en © The Author(s), under exclusive licence to International Society for Microbial Ecology 2020
spellingShingle Article
Martin, Marivic
Dragoš, Anna
Otto, Simon B.
Schäfer, Daniel
Brix, Susanne
Maróti, Gergely
Kovács, Ákos T.
Cheaters shape the evolution of phenotypic heterogeneity in Bacillus subtilis biofilms
title Cheaters shape the evolution of phenotypic heterogeneity in Bacillus subtilis biofilms
title_full Cheaters shape the evolution of phenotypic heterogeneity in Bacillus subtilis biofilms
title_fullStr Cheaters shape the evolution of phenotypic heterogeneity in Bacillus subtilis biofilms
title_full_unstemmed Cheaters shape the evolution of phenotypic heterogeneity in Bacillus subtilis biofilms
title_short Cheaters shape the evolution of phenotypic heterogeneity in Bacillus subtilis biofilms
title_sort cheaters shape the evolution of phenotypic heterogeneity in bacillus subtilis biofilms
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7608354/
https://www.ncbi.nlm.nih.gov/pubmed/32483306
http://dx.doi.org/10.1038/s41396-020-0685-4
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