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Competition between growth and shear stress drives intermittency in preferential flow paths in porous medium biofilms

Bacteria in porous media, such as soils, aquifers, and filters, often form surface-attached communities known as biofilms. Biofilms are affected by fluid flow through the porous medium, for example, for nutrient supply, and they, in turn, affect the flow. A striking example of this interplay is the...

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Autores principales: Kurz, Dorothee L., Secchi, Eleonora, Carrillo, Francisco J., Bourg, Ian C., Stocker, Roman, Jimenez-Martinez, Joaquin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9335220/
https://www.ncbi.nlm.nih.gov/pubmed/35858419
http://dx.doi.org/10.1073/pnas.2122202119
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author Kurz, Dorothee L.
Secchi, Eleonora
Carrillo, Francisco J.
Bourg, Ian C.
Stocker, Roman
Jimenez-Martinez, Joaquin
author_facet Kurz, Dorothee L.
Secchi, Eleonora
Carrillo, Francisco J.
Bourg, Ian C.
Stocker, Roman
Jimenez-Martinez, Joaquin
author_sort Kurz, Dorothee L.
collection PubMed
description Bacteria in porous media, such as soils, aquifers, and filters, often form surface-attached communities known as biofilms. Biofilms are affected by fluid flow through the porous medium, for example, for nutrient supply, and they, in turn, affect the flow. A striking example of this interplay is the strong intermittency in flow that can occur when biofilms nearly clog the porous medium. Intermittency manifests itself as the rapid opening and slow closing of individual preferential flow paths (PFPs) through the biofilm–porous medium structure, leading to continual spatiotemporal rearrangement. The drastic changes to the flow and mass transport induced by intermittency can affect the functioning and efficiency of natural and industrial systems. Yet, the mechanistic origin of intermittency remains unexplained. Here, we show that the mechanism driving PFP intermittency is the competition between microbial growth and shear stress. We combined microfluidic experiments quantifying Bacillus subtilis biofilm formation and behavior in synthetic porous media for different pore sizes and flow rates with a mathematical model accounting for flow through the biofilm and biofilm poroelasticity to reveal the underlying mechanisms. We show that the closing of PFPs is driven by microbial growth, controlled by nutrient mass flow. Opposing this, we find that the opening of PFPs is driven by flow-induced shear stress, which increases as a PFP becomes narrower due to microbial growth, causing biofilm compression and rupture. Our results demonstrate that microbial growth and its competition with shear stresses can lead to strong temporal variability in flow and transport conditions in bioclogged porous media.
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spelling pubmed-93352202023-01-18 Competition between growth and shear stress drives intermittency in preferential flow paths in porous medium biofilms Kurz, Dorothee L. Secchi, Eleonora Carrillo, Francisco J. Bourg, Ian C. Stocker, Roman Jimenez-Martinez, Joaquin Proc Natl Acad Sci U S A Physical Sciences Bacteria in porous media, such as soils, aquifers, and filters, often form surface-attached communities known as biofilms. Biofilms are affected by fluid flow through the porous medium, for example, for nutrient supply, and they, in turn, affect the flow. A striking example of this interplay is the strong intermittency in flow that can occur when biofilms nearly clog the porous medium. Intermittency manifests itself as the rapid opening and slow closing of individual preferential flow paths (PFPs) through the biofilm–porous medium structure, leading to continual spatiotemporal rearrangement. The drastic changes to the flow and mass transport induced by intermittency can affect the functioning and efficiency of natural and industrial systems. Yet, the mechanistic origin of intermittency remains unexplained. Here, we show that the mechanism driving PFP intermittency is the competition between microbial growth and shear stress. We combined microfluidic experiments quantifying Bacillus subtilis biofilm formation and behavior in synthetic porous media for different pore sizes and flow rates with a mathematical model accounting for flow through the biofilm and biofilm poroelasticity to reveal the underlying mechanisms. We show that the closing of PFPs is driven by microbial growth, controlled by nutrient mass flow. Opposing this, we find that the opening of PFPs is driven by flow-induced shear stress, which increases as a PFP becomes narrower due to microbial growth, causing biofilm compression and rupture. Our results demonstrate that microbial growth and its competition with shear stresses can lead to strong temporal variability in flow and transport conditions in bioclogged porous media. National Academy of Sciences 2022-07-18 2022-07-26 /pmc/articles/PMC9335220/ /pubmed/35858419 http://dx.doi.org/10.1073/pnas.2122202119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Physical Sciences
Kurz, Dorothee L.
Secchi, Eleonora
Carrillo, Francisco J.
Bourg, Ian C.
Stocker, Roman
Jimenez-Martinez, Joaquin
Competition between growth and shear stress drives intermittency in preferential flow paths in porous medium biofilms
title Competition between growth and shear stress drives intermittency in preferential flow paths in porous medium biofilms
title_full Competition between growth and shear stress drives intermittency in preferential flow paths in porous medium biofilms
title_fullStr Competition between growth and shear stress drives intermittency in preferential flow paths in porous medium biofilms
title_full_unstemmed Competition between growth and shear stress drives intermittency in preferential flow paths in porous medium biofilms
title_short Competition between growth and shear stress drives intermittency in preferential flow paths in porous medium biofilms
title_sort competition between growth and shear stress drives intermittency in preferential flow paths in porous medium biofilms
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9335220/
https://www.ncbi.nlm.nih.gov/pubmed/35858419
http://dx.doi.org/10.1073/pnas.2122202119
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