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Flow environment and matrix structure interact to determine spatial competition in Pseudomonas aeruginosa biofilms

Bacteria often live in biofilms, which are microbial communities surrounded by a secreted extracellular matrix. Here, we demonstrate that hydrodynamic flow and matrix organization interact to shape competitive dynamics in Pseudomonas aeruginosa biofilms. Irrespective of initial frequency, in competi...

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Autores principales: Nadell, Carey D, Ricaurte, Deirdre, Yan, Jing, Drescher, Knut, Bassler, Bonnie L
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5283829/
https://www.ncbi.nlm.nih.gov/pubmed/28084994
http://dx.doi.org/10.7554/eLife.21855
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author Nadell, Carey D
Ricaurte, Deirdre
Yan, Jing
Drescher, Knut
Bassler, Bonnie L
author_facet Nadell, Carey D
Ricaurte, Deirdre
Yan, Jing
Drescher, Knut
Bassler, Bonnie L
author_sort Nadell, Carey D
collection PubMed
description Bacteria often live in biofilms, which are microbial communities surrounded by a secreted extracellular matrix. Here, we demonstrate that hydrodynamic flow and matrix organization interact to shape competitive dynamics in Pseudomonas aeruginosa biofilms. Irrespective of initial frequency, in competition with matrix mutants, wild-type cells always increase in relative abundance in planar microfluidic devices under simple flow regimes. By contrast, in microenvironments with complex, irregular flow profiles – which are common in natural environments – wild-type matrix-producing and isogenic non-producing strains can coexist. This result stems from local obstruction of flow by wild-type matrix producers, which generates regions of near-zero shear that allow matrix mutants to locally accumulate. Our findings connect the evolutionary stability of matrix production with the hydrodynamics and spatial structure of the surrounding environment, providing a potential explanation for the variation in biofilm matrix secretion observed among bacteria in natural environments. DOI: http://dx.doi.org/10.7554/eLife.21855.001
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spelling pubmed-52838292017-02-01 Flow environment and matrix structure interact to determine spatial competition in Pseudomonas aeruginosa biofilms Nadell, Carey D Ricaurte, Deirdre Yan, Jing Drescher, Knut Bassler, Bonnie L eLife Ecology Bacteria often live in biofilms, which are microbial communities surrounded by a secreted extracellular matrix. Here, we demonstrate that hydrodynamic flow and matrix organization interact to shape competitive dynamics in Pseudomonas aeruginosa biofilms. Irrespective of initial frequency, in competition with matrix mutants, wild-type cells always increase in relative abundance in planar microfluidic devices under simple flow regimes. By contrast, in microenvironments with complex, irregular flow profiles – which are common in natural environments – wild-type matrix-producing and isogenic non-producing strains can coexist. This result stems from local obstruction of flow by wild-type matrix producers, which generates regions of near-zero shear that allow matrix mutants to locally accumulate. Our findings connect the evolutionary stability of matrix production with the hydrodynamics and spatial structure of the surrounding environment, providing a potential explanation for the variation in biofilm matrix secretion observed among bacteria in natural environments. DOI: http://dx.doi.org/10.7554/eLife.21855.001 eLife Sciences Publications, Ltd 2017-01-13 /pmc/articles/PMC5283829/ /pubmed/28084994 http://dx.doi.org/10.7554/eLife.21855 Text en © 2017, Nadell et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Ecology
Nadell, Carey D
Ricaurte, Deirdre
Yan, Jing
Drescher, Knut
Bassler, Bonnie L
Flow environment and matrix structure interact to determine spatial competition in Pseudomonas aeruginosa biofilms
title Flow environment and matrix structure interact to determine spatial competition in Pseudomonas aeruginosa biofilms
title_full Flow environment and matrix structure interact to determine spatial competition in Pseudomonas aeruginosa biofilms
title_fullStr Flow environment and matrix structure interact to determine spatial competition in Pseudomonas aeruginosa biofilms
title_full_unstemmed Flow environment and matrix structure interact to determine spatial competition in Pseudomonas aeruginosa biofilms
title_short Flow environment and matrix structure interact to determine spatial competition in Pseudomonas aeruginosa biofilms
title_sort flow environment and matrix structure interact to determine spatial competition in pseudomonas aeruginosa biofilms
topic Ecology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5283829/
https://www.ncbi.nlm.nih.gov/pubmed/28084994
http://dx.doi.org/10.7554/eLife.21855
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