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Shared biophysical mechanisms determine early biofilm architecture development across different bacterial species

Bacterial biofilms are among the most abundant multicellular structures on Earth and play essential roles in a wide range of ecological, medical, and industrial processes. However, general principles that govern the emergence of biofilm architecture across different species remain unknown. Here, we...

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Autores principales: Jeckel, Hannah, Díaz-Pascual, Francisco, Skinner, Dominic J., Song, Boya, Jiménez-Siebert, Eva, Strenger, Kerstin, Jelli, Eric, Vaidya, Sanika, Dunkel, Jörn, Drescher, Knut
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9605341/
https://www.ncbi.nlm.nih.gov/pubmed/36288405
http://dx.doi.org/10.1371/journal.pbio.3001846
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author Jeckel, Hannah
Díaz-Pascual, Francisco
Skinner, Dominic J.
Song, Boya
Jiménez-Siebert, Eva
Strenger, Kerstin
Jelli, Eric
Vaidya, Sanika
Dunkel, Jörn
Drescher, Knut
author_facet Jeckel, Hannah
Díaz-Pascual, Francisco
Skinner, Dominic J.
Song, Boya
Jiménez-Siebert, Eva
Strenger, Kerstin
Jelli, Eric
Vaidya, Sanika
Dunkel, Jörn
Drescher, Knut
author_sort Jeckel, Hannah
collection PubMed
description Bacterial biofilms are among the most abundant multicellular structures on Earth and play essential roles in a wide range of ecological, medical, and industrial processes. However, general principles that govern the emergence of biofilm architecture across different species remain unknown. Here, we combine experiments, simulations, and statistical analysis to identify shared biophysical mechanisms that determine early biofilm architecture development at the single-cell level, for the species Vibrio cholerae, Escherichia coli, Salmonella enterica, and Pseudomonas aeruginosa grown as microcolonies in flow chambers. Our data-driven analysis reveals that despite the many molecular differences between these species, the biofilm architecture differences can be described by only 2 control parameters: cellular aspect ratio and cell density. Further experiments using single-species mutants for which the cell aspect ratio and the cell density are systematically varied, and mechanistic simulations show that tuning these 2 control parameters reproduces biofilm architectures of different species. Altogether, our results show that biofilm microcolony architecture is determined by mechanical cell–cell interactions, which are conserved across different species.
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spelling pubmed-96053412022-10-27 Shared biophysical mechanisms determine early biofilm architecture development across different bacterial species Jeckel, Hannah Díaz-Pascual, Francisco Skinner, Dominic J. Song, Boya Jiménez-Siebert, Eva Strenger, Kerstin Jelli, Eric Vaidya, Sanika Dunkel, Jörn Drescher, Knut PLoS Biol Research Article Bacterial biofilms are among the most abundant multicellular structures on Earth and play essential roles in a wide range of ecological, medical, and industrial processes. However, general principles that govern the emergence of biofilm architecture across different species remain unknown. Here, we combine experiments, simulations, and statistical analysis to identify shared biophysical mechanisms that determine early biofilm architecture development at the single-cell level, for the species Vibrio cholerae, Escherichia coli, Salmonella enterica, and Pseudomonas aeruginosa grown as microcolonies in flow chambers. Our data-driven analysis reveals that despite the many molecular differences between these species, the biofilm architecture differences can be described by only 2 control parameters: cellular aspect ratio and cell density. Further experiments using single-species mutants for which the cell aspect ratio and the cell density are systematically varied, and mechanistic simulations show that tuning these 2 control parameters reproduces biofilm architectures of different species. Altogether, our results show that biofilm microcolony architecture is determined by mechanical cell–cell interactions, which are conserved across different species. Public Library of Science 2022-10-26 /pmc/articles/PMC9605341/ /pubmed/36288405 http://dx.doi.org/10.1371/journal.pbio.3001846 Text en © 2022 Jeckel et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Jeckel, Hannah
Díaz-Pascual, Francisco
Skinner, Dominic J.
Song, Boya
Jiménez-Siebert, Eva
Strenger, Kerstin
Jelli, Eric
Vaidya, Sanika
Dunkel, Jörn
Drescher, Knut
Shared biophysical mechanisms determine early biofilm architecture development across different bacterial species
title Shared biophysical mechanisms determine early biofilm architecture development across different bacterial species
title_full Shared biophysical mechanisms determine early biofilm architecture development across different bacterial species
title_fullStr Shared biophysical mechanisms determine early biofilm architecture development across different bacterial species
title_full_unstemmed Shared biophysical mechanisms determine early biofilm architecture development across different bacterial species
title_short Shared biophysical mechanisms determine early biofilm architecture development across different bacterial species
title_sort shared biophysical mechanisms determine early biofilm architecture development across different bacterial species
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9605341/
https://www.ncbi.nlm.nih.gov/pubmed/36288405
http://dx.doi.org/10.1371/journal.pbio.3001846
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