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Self-Driven Jamming in Growing Microbial Populations

In natural settings, microbes tend to grow in dense populations [1–4] where they need to push against their surroundings to accommodate space for new cells. The associated contact forces play a critical role in a variety of population-level processes, including biofilm formation [5–7], the colonizat...

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Autores principales: Delarue, Morgan, Hartung, Jörn, Schreck, Carl, Gniewek, Pawel, Hu, Lucy, Herminghaus, Stephan, Hallatschek, Oskar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5022770/
https://www.ncbi.nlm.nih.gov/pubmed/27642362
http://dx.doi.org/10.1038/nphys3741
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author Delarue, Morgan
Hartung, Jörn
Schreck, Carl
Gniewek, Pawel
Hu, Lucy
Herminghaus, Stephan
Hallatschek, Oskar
author_facet Delarue, Morgan
Hartung, Jörn
Schreck, Carl
Gniewek, Pawel
Hu, Lucy
Herminghaus, Stephan
Hallatschek, Oskar
author_sort Delarue, Morgan
collection PubMed
description In natural settings, microbes tend to grow in dense populations [1–4] where they need to push against their surroundings to accommodate space for new cells. The associated contact forces play a critical role in a variety of population-level processes, including biofilm formation [5–7], the colonization of porous media [8, 9], and the invasion of biological tissues [10–12]. Although mechanical forces have been characterized at the single cell level [13–16], it remains elusive how collective pushing forces result from the combination of single cell forces. Here, we reveal a collective mechanism of confinement, which we call self-driven jamming, that promotes the build-up of large mechanical pressures in microbial populations. Microfluidic experiments on budding yeast populations in space-limited environments show that self-driven jamming arises from the gradual formation and sudden collapse of force chains driven by microbial proliferation, extending the framework of driven granular matter [17–20]. The resulting contact pressures can become large enough to slow down cell growth, to delay the cell cycle in the G1 phase, and to strain or even destroy the microenvironment through crack propagation. Our results suggest that self-driven jamming and build-up of large mechanical pressures is a natural tendency of microbes growing in confined spaces, contributing to microbial pathogenesis and biofouling [21–26].
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spelling pubmed-50227702016-11-09 Self-Driven Jamming in Growing Microbial Populations Delarue, Morgan Hartung, Jörn Schreck, Carl Gniewek, Pawel Hu, Lucy Herminghaus, Stephan Hallatschek, Oskar Nat Phys Article In natural settings, microbes tend to grow in dense populations [1–4] where they need to push against their surroundings to accommodate space for new cells. The associated contact forces play a critical role in a variety of population-level processes, including biofilm formation [5–7], the colonization of porous media [8, 9], and the invasion of biological tissues [10–12]. Although mechanical forces have been characterized at the single cell level [13–16], it remains elusive how collective pushing forces result from the combination of single cell forces. Here, we reveal a collective mechanism of confinement, which we call self-driven jamming, that promotes the build-up of large mechanical pressures in microbial populations. Microfluidic experiments on budding yeast populations in space-limited environments show that self-driven jamming arises from the gradual formation and sudden collapse of force chains driven by microbial proliferation, extending the framework of driven granular matter [17–20]. The resulting contact pressures can become large enough to slow down cell growth, to delay the cell cycle in the G1 phase, and to strain or even destroy the microenvironment through crack propagation. Our results suggest that self-driven jamming and build-up of large mechanical pressures is a natural tendency of microbes growing in confined spaces, contributing to microbial pathogenesis and biofouling [21–26]. 2016-05-09 2016-08 /pmc/articles/PMC5022770/ /pubmed/27642362 http://dx.doi.org/10.1038/nphys3741 Text en 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
Delarue, Morgan
Hartung, Jörn
Schreck, Carl
Gniewek, Pawel
Hu, Lucy
Herminghaus, Stephan
Hallatschek, Oskar
Self-Driven Jamming in Growing Microbial Populations
title Self-Driven Jamming in Growing Microbial Populations
title_full Self-Driven Jamming in Growing Microbial Populations
title_fullStr Self-Driven Jamming in Growing Microbial Populations
title_full_unstemmed Self-Driven Jamming in Growing Microbial Populations
title_short Self-Driven Jamming in Growing Microbial Populations
title_sort self-driven jamming in growing microbial populations
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5022770/
https://www.ncbi.nlm.nih.gov/pubmed/27642362
http://dx.doi.org/10.1038/nphys3741
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