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Signaling in microbial communities with open boundaries

Microbial communities such as swarms or biofilms often form at the interfaces of solid substrates and open fluid flows. At the same time, in laboratory environments these communities are commonly studied using microfluidic devices with media flows and open boundaries. Extracellular signaling within...

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Autores principales: Winkle, James J., Saha, Soutick, Essman, Joseph, Bennett, Matthew R., Ott, William, Josić, Krešimir, Mugler, Andrew
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9882294/
https://www.ncbi.nlm.nih.gov/pubmed/36711825
http://dx.doi.org/10.1101/2023.01.20.524904
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author Winkle, James J.
Saha, Soutick
Essman, Joseph
Bennett, Matthew R.
Ott, William
Josić, Krešimir
Mugler, Andrew
author_facet Winkle, James J.
Saha, Soutick
Essman, Joseph
Bennett, Matthew R.
Ott, William
Josić, Krešimir
Mugler, Andrew
author_sort Winkle, James J.
collection PubMed
description Microbial communities such as swarms or biofilms often form at the interfaces of solid substrates and open fluid flows. At the same time, in laboratory environments these communities are commonly studied using microfluidic devices with media flows and open boundaries. Extracellular signaling within these communities is therefore subject to different constraints than signaling within classic, closed-boundary systems such as developing embryos or tissues, yet is understudied by comparison. Here, we use mathematical modeling to show how advective-diffusive boundary flows and population geometry impact cell-cell signaling in monolayer microbial communities. We reveal conditions where the intercellular signaling lengthscale depends solely on the population geometry and not on diffusion or degradation, as commonly expected. We further demonstrate that diffusive coupling with the boundary flow can produce signal gradients within an isogenic population, even when there is no flow within the population. We use our theory to provide new insights into the signaling mechanisms of published experimental results, and we make several experimentally verifiable predictions. Our research highlights the importance of carefully evaluating boundary dynamics and environmental geometry when modeling microbial cell-cell signaling and informs the study of cell behaviors in both natural and synthetic systems.
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spelling pubmed-98822942023-01-28 Signaling in microbial communities with open boundaries Winkle, James J. Saha, Soutick Essman, Joseph Bennett, Matthew R. Ott, William Josić, Krešimir Mugler, Andrew bioRxiv Article Microbial communities such as swarms or biofilms often form at the interfaces of solid substrates and open fluid flows. At the same time, in laboratory environments these communities are commonly studied using microfluidic devices with media flows and open boundaries. Extracellular signaling within these communities is therefore subject to different constraints than signaling within classic, closed-boundary systems such as developing embryos or tissues, yet is understudied by comparison. Here, we use mathematical modeling to show how advective-diffusive boundary flows and population geometry impact cell-cell signaling in monolayer microbial communities. We reveal conditions where the intercellular signaling lengthscale depends solely on the population geometry and not on diffusion or degradation, as commonly expected. We further demonstrate that diffusive coupling with the boundary flow can produce signal gradients within an isogenic population, even when there is no flow within the population. We use our theory to provide new insights into the signaling mechanisms of published experimental results, and we make several experimentally verifiable predictions. Our research highlights the importance of carefully evaluating boundary dynamics and environmental geometry when modeling microbial cell-cell signaling and informs the study of cell behaviors in both natural and synthetic systems. Cold Spring Harbor Laboratory 2023-01-20 /pmc/articles/PMC9882294/ /pubmed/36711825 http://dx.doi.org/10.1101/2023.01.20.524904 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Winkle, James J.
Saha, Soutick
Essman, Joseph
Bennett, Matthew R.
Ott, William
Josić, Krešimir
Mugler, Andrew
Signaling in microbial communities with open boundaries
title Signaling in microbial communities with open boundaries
title_full Signaling in microbial communities with open boundaries
title_fullStr Signaling in microbial communities with open boundaries
title_full_unstemmed Signaling in microbial communities with open boundaries
title_short Signaling in microbial communities with open boundaries
title_sort signaling in microbial communities with open boundaries
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9882294/
https://www.ncbi.nlm.nih.gov/pubmed/36711825
http://dx.doi.org/10.1101/2023.01.20.524904
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