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Breakdown of Vibrio cholerae biofilm architecture induced by antibiotics disrupts community barrier function

Bacterial cells in nature are frequently exposed to changes in their chemical environment(1,2). For such stimuli, the response mechanisms of isolated cells have been investigated in great detail. By contrast, little is known about the emergent multicellular responses to environmental changes, such a...

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Autores principales: Díaz-Pascual, Francisco, Hartmann, Raimo, Lempp, Martin, Vidakovic, Lucia, Song, Boya, Jeckel, Hannah, Thormann, Kai M., Yildiz, Fitnat H., Dunkel, Jörn, Link, Hannes, Nadell, Carey D., Drescher, Knut
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6881181/
https://www.ncbi.nlm.nih.gov/pubmed/31659297
http://dx.doi.org/10.1038/s41564-019-0579-2
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author Díaz-Pascual, Francisco
Hartmann, Raimo
Lempp, Martin
Vidakovic, Lucia
Song, Boya
Jeckel, Hannah
Thormann, Kai M.
Yildiz, Fitnat H.
Dunkel, Jörn
Link, Hannes
Nadell, Carey D.
Drescher, Knut
author_facet Díaz-Pascual, Francisco
Hartmann, Raimo
Lempp, Martin
Vidakovic, Lucia
Song, Boya
Jeckel, Hannah
Thormann, Kai M.
Yildiz, Fitnat H.
Dunkel, Jörn
Link, Hannes
Nadell, Carey D.
Drescher, Knut
author_sort Díaz-Pascual, Francisco
collection PubMed
description Bacterial cells in nature are frequently exposed to changes in their chemical environment(1,2). For such stimuli, the response mechanisms of isolated cells have been investigated in great detail. By contrast, little is known about the emergent multicellular responses to environmental changes, such as antibiotic exposure(3–7), which may hold the key to understanding the structure and functions of the most common bacterial communities: biofilms. Here, by monitoring all individual cells in Vibrio cholerae biofilms during exposure to commonly administered antibiotics for cholera infections, we discovered that translational inhibitors cause strong effects on cell size and shape, as well as biofilm architectural properties. We identified that single-cell-level responses result from the metabolic consequences of protein synthesis inhibition, and that the community-level responses result from an interplay of matrix composition, matrix dissociation, and mechanical interactions between cells. We further discovered that the antibiotic-induced changes in biofilm architecture have substantial effects on biofilm population dynamics and community assembly, by enabling invasion of biofilms by bacteriophages and intruder cells of different species. These mechanistic causes and ecological consequences of biofilm exposure to antibiotics are an important step towards understanding collective bacterial responses to environmental changes, with implications for the effects of antimicrobial therapy on the ecological succession of biofilm communities.
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spelling pubmed-68811812020-04-28 Breakdown of Vibrio cholerae biofilm architecture induced by antibiotics disrupts community barrier function Díaz-Pascual, Francisco Hartmann, Raimo Lempp, Martin Vidakovic, Lucia Song, Boya Jeckel, Hannah Thormann, Kai M. Yildiz, Fitnat H. Dunkel, Jörn Link, Hannes Nadell, Carey D. Drescher, Knut Nat Microbiol Article Bacterial cells in nature are frequently exposed to changes in their chemical environment(1,2). For such stimuli, the response mechanisms of isolated cells have been investigated in great detail. By contrast, little is known about the emergent multicellular responses to environmental changes, such as antibiotic exposure(3–7), which may hold the key to understanding the structure and functions of the most common bacterial communities: biofilms. Here, by monitoring all individual cells in Vibrio cholerae biofilms during exposure to commonly administered antibiotics for cholera infections, we discovered that translational inhibitors cause strong effects on cell size and shape, as well as biofilm architectural properties. We identified that single-cell-level responses result from the metabolic consequences of protein synthesis inhibition, and that the community-level responses result from an interplay of matrix composition, matrix dissociation, and mechanical interactions between cells. We further discovered that the antibiotic-induced changes in biofilm architecture have substantial effects on biofilm population dynamics and community assembly, by enabling invasion of biofilms by bacteriophages and intruder cells of different species. These mechanistic causes and ecological consequences of biofilm exposure to antibiotics are an important step towards understanding collective bacterial responses to environmental changes, with implications for the effects of antimicrobial therapy on the ecological succession of biofilm communities. 2019-10-28 2019-12 /pmc/articles/PMC6881181/ /pubmed/31659297 http://dx.doi.org/10.1038/s41564-019-0579-2 Text en http://www.nature.com/authors/editorial_policies/license.html#terms Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
Díaz-Pascual, Francisco
Hartmann, Raimo
Lempp, Martin
Vidakovic, Lucia
Song, Boya
Jeckel, Hannah
Thormann, Kai M.
Yildiz, Fitnat H.
Dunkel, Jörn
Link, Hannes
Nadell, Carey D.
Drescher, Knut
Breakdown of Vibrio cholerae biofilm architecture induced by antibiotics disrupts community barrier function
title Breakdown of Vibrio cholerae biofilm architecture induced by antibiotics disrupts community barrier function
title_full Breakdown of Vibrio cholerae biofilm architecture induced by antibiotics disrupts community barrier function
title_fullStr Breakdown of Vibrio cholerae biofilm architecture induced by antibiotics disrupts community barrier function
title_full_unstemmed Breakdown of Vibrio cholerae biofilm architecture induced by antibiotics disrupts community barrier function
title_short Breakdown of Vibrio cholerae biofilm architecture induced by antibiotics disrupts community barrier function
title_sort breakdown of vibrio cholerae biofilm architecture induced by antibiotics disrupts community barrier function
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6881181/
https://www.ncbi.nlm.nih.gov/pubmed/31659297
http://dx.doi.org/10.1038/s41564-019-0579-2
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