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Social evolution of shared biofilm matrix components

Biofilm formation is an important and ubiquitous mode of growth among bacteria. Central to the evolutionary advantage of biofilm formation is cell–cell and cell–surface adhesion achieved by a variety of factors, some of which are diffusible compounds that may operate as classical public goods—factor...

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Autores principales: Tai, Jung-Shen B., Mukherjee, Saikat, Nero, Thomas, Olson, Rich, Tithof, Jeffrey, Nadell, Carey D., Yan, Jing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9271185/
https://www.ncbi.nlm.nih.gov/pubmed/35771939
http://dx.doi.org/10.1073/pnas.2123469119
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author Tai, Jung-Shen B.
Mukherjee, Saikat
Nero, Thomas
Olson, Rich
Tithof, Jeffrey
Nadell, Carey D.
Yan, Jing
author_facet Tai, Jung-Shen B.
Mukherjee, Saikat
Nero, Thomas
Olson, Rich
Tithof, Jeffrey
Nadell, Carey D.
Yan, Jing
author_sort Tai, Jung-Shen B.
collection PubMed
description Biofilm formation is an important and ubiquitous mode of growth among bacteria. Central to the evolutionary advantage of biofilm formation is cell–cell and cell–surface adhesion achieved by a variety of factors, some of which are diffusible compounds that may operate as classical public goods—factors that are costly to produce but may benefit other cells. An outstanding question is how diffusible matrix production, in general, can be stable over evolutionary timescales. In this work, using Vibrio cholerae as a model, we show that shared diffusible biofilm matrix proteins are indeed susceptible to cheater exploitation and that the evolutionary stability of producing these matrix components fundamentally depends on biofilm spatial structure, intrinsic sharing mechanisms of these components, and flow conditions in the environment. We further show that exploitation of diffusible adhesion proteins is localized within a well-defined spatial range around cell clusters that produce them. Based on this exploitation range and the spatial distribution of cell clusters, we constructed a model of costly diffusible matrix production and related these length scales to the relatedness coefficient in social evolution theory. Our results show that production of diffusible biofilm matrix components is evolutionarily stable under conditions consistent with natural biofilm habitats and host environments. We expect the mechanisms revealed in this study to be relevant to other secreted factors that operate as cooperative public goods in bacterial communities and the concept of exploitation range and the associated analysis tools to be generally applicable.
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spelling pubmed-92711852022-12-30 Social evolution of shared biofilm matrix components Tai, Jung-Shen B. Mukherjee, Saikat Nero, Thomas Olson, Rich Tithof, Jeffrey Nadell, Carey D. Yan, Jing Proc Natl Acad Sci U S A Biological Sciences Biofilm formation is an important and ubiquitous mode of growth among bacteria. Central to the evolutionary advantage of biofilm formation is cell–cell and cell–surface adhesion achieved by a variety of factors, some of which are diffusible compounds that may operate as classical public goods—factors that are costly to produce but may benefit other cells. An outstanding question is how diffusible matrix production, in general, can be stable over evolutionary timescales. In this work, using Vibrio cholerae as a model, we show that shared diffusible biofilm matrix proteins are indeed susceptible to cheater exploitation and that the evolutionary stability of producing these matrix components fundamentally depends on biofilm spatial structure, intrinsic sharing mechanisms of these components, and flow conditions in the environment. We further show that exploitation of diffusible adhesion proteins is localized within a well-defined spatial range around cell clusters that produce them. Based on this exploitation range and the spatial distribution of cell clusters, we constructed a model of costly diffusible matrix production and related these length scales to the relatedness coefficient in social evolution theory. Our results show that production of diffusible biofilm matrix components is evolutionarily stable under conditions consistent with natural biofilm habitats and host environments. We expect the mechanisms revealed in this study to be relevant to other secreted factors that operate as cooperative public goods in bacterial communities and the concept of exploitation range and the associated analysis tools to be generally applicable. National Academy of Sciences 2022-06-30 2022-07-05 /pmc/articles/PMC9271185/ /pubmed/35771939 http://dx.doi.org/10.1073/pnas.2123469119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Tai, Jung-Shen B.
Mukherjee, Saikat
Nero, Thomas
Olson, Rich
Tithof, Jeffrey
Nadell, Carey D.
Yan, Jing
Social evolution of shared biofilm matrix components
title Social evolution of shared biofilm matrix components
title_full Social evolution of shared biofilm matrix components
title_fullStr Social evolution of shared biofilm matrix components
title_full_unstemmed Social evolution of shared biofilm matrix components
title_short Social evolution of shared biofilm matrix components
title_sort social evolution of shared biofilm matrix components
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9271185/
https://www.ncbi.nlm.nih.gov/pubmed/35771939
http://dx.doi.org/10.1073/pnas.2123469119
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