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Biofilm formation and toxin production provide a fitness advantage in mixed colonies of environmental yeast isolates

Microbes can engage in social interactions ranging from cooperation to warfare. Biofilms are structured, cooperative microbial communities. Like all cooperative communities, they are susceptible to invasion by selfish individuals who benefit without contributing. However, biofilms are pervasive and...

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Autores principales: Deschaine, Bernadette M., Heysel, Angela R., Lenhart, B. Adam, Murphy, Helen A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6010761/
https://www.ncbi.nlm.nih.gov/pubmed/29938072
http://dx.doi.org/10.1002/ece3.4082
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author Deschaine, Bernadette M.
Heysel, Angela R.
Lenhart, B. Adam
Murphy, Helen A.
author_facet Deschaine, Bernadette M.
Heysel, Angela R.
Lenhart, B. Adam
Murphy, Helen A.
author_sort Deschaine, Bernadette M.
collection PubMed
description Microbes can engage in social interactions ranging from cooperation to warfare. Biofilms are structured, cooperative microbial communities. Like all cooperative communities, they are susceptible to invasion by selfish individuals who benefit without contributing. However, biofilms are pervasive and ancient, representing the first fossilized life. One hypothesis for the stability of biofilms is spatial structure: Segregated patches of related cooperative cells are able to outcompete unrelated cells. These dynamics have been explored computationally and in bacteria; however, their relevance to eukaryotic microbes remains an open question. The complexity of eukaryotic cell signaling and communication suggests the possibility of different social dynamics. Using the tractable model yeast, Saccharomyces cerevisiae, which can form biofilms, we investigate the interactions of environmental isolates with different social phenotypes. We find that biofilm strains spatially exclude nonbiofilm strains and that biofilm spatial structure confers a consistent and robust fitness advantage in direct competition. Furthermore, biofilms may protect against killer toxin, a warfare phenotype. During biofilm formation, cells are susceptible to toxin from nearby competitors; however, increased spatial use may provide an escape from toxin producers. Our results suggest that yeast biofilms represent a competitive strategy and that principles elucidated for the evolution and stability of bacterial biofilms may apply to more complex eukaryotes.
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spelling pubmed-60107612018-06-22 Biofilm formation and toxin production provide a fitness advantage in mixed colonies of environmental yeast isolates Deschaine, Bernadette M. Heysel, Angela R. Lenhart, B. Adam Murphy, Helen A. Ecol Evol Original Research Microbes can engage in social interactions ranging from cooperation to warfare. Biofilms are structured, cooperative microbial communities. Like all cooperative communities, they are susceptible to invasion by selfish individuals who benefit without contributing. However, biofilms are pervasive and ancient, representing the first fossilized life. One hypothesis for the stability of biofilms is spatial structure: Segregated patches of related cooperative cells are able to outcompete unrelated cells. These dynamics have been explored computationally and in bacteria; however, their relevance to eukaryotic microbes remains an open question. The complexity of eukaryotic cell signaling and communication suggests the possibility of different social dynamics. Using the tractable model yeast, Saccharomyces cerevisiae, which can form biofilms, we investigate the interactions of environmental isolates with different social phenotypes. We find that biofilm strains spatially exclude nonbiofilm strains and that biofilm spatial structure confers a consistent and robust fitness advantage in direct competition. Furthermore, biofilms may protect against killer toxin, a warfare phenotype. During biofilm formation, cells are susceptible to toxin from nearby competitors; however, increased spatial use may provide an escape from toxin producers. Our results suggest that yeast biofilms represent a competitive strategy and that principles elucidated for the evolution and stability of bacterial biofilms may apply to more complex eukaryotes. John Wiley and Sons Inc. 2018-04-27 /pmc/articles/PMC6010761/ /pubmed/29938072 http://dx.doi.org/10.1002/ece3.4082 Text en © 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Deschaine, Bernadette M.
Heysel, Angela R.
Lenhart, B. Adam
Murphy, Helen A.
Biofilm formation and toxin production provide a fitness advantage in mixed colonies of environmental yeast isolates
title Biofilm formation and toxin production provide a fitness advantage in mixed colonies of environmental yeast isolates
title_full Biofilm formation and toxin production provide a fitness advantage in mixed colonies of environmental yeast isolates
title_fullStr Biofilm formation and toxin production provide a fitness advantage in mixed colonies of environmental yeast isolates
title_full_unstemmed Biofilm formation and toxin production provide a fitness advantage in mixed colonies of environmental yeast isolates
title_short Biofilm formation and toxin production provide a fitness advantage in mixed colonies of environmental yeast isolates
title_sort biofilm formation and toxin production provide a fitness advantage in mixed colonies of environmental yeast isolates
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6010761/
https://www.ncbi.nlm.nih.gov/pubmed/29938072
http://dx.doi.org/10.1002/ece3.4082
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