Agent-Based Modeling Demonstrates How Local Chemotactic Behavior Can Shape Biofilm Architecture

ABSTRACT Bacteria are often found living in aggregated multicellular communities known as biofilms. Biofilms are three-dimensional structures that confer distinct physical and biological properties to the collective of cells living within them. We used agent-based modeling to explore whether local c...

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Autores principales:	Emily G. Sweeney, Andrew Nishida, Alexandra Weston, Maria S. Bañuelos, Kristin Potter, John Conery, Karen Guillemin
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	autoinducer 2 biofilms chemotaxis computer modeling Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d3c261acaab04c50b6951dc6de6ec08f
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spelling	oai:doaj.org-article:d3c261acaab04c50b6951dc6de6ec08f2021-11-15T15:22:20ZAgent-Based Modeling Demonstrates How Local Chemotactic Behavior Can Shape Biofilm Architecture10.1128/mSphere.00285-192379-5042https://doaj.org/article/d3c261acaab04c50b6951dc6de6ec08f2019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00285-19https://doaj.org/toc/2379-5042ABSTRACT Bacteria are often found living in aggregated multicellular communities known as biofilms. Biofilms are three-dimensional structures that confer distinct physical and biological properties to the collective of cells living within them. We used agent-based modeling to explore whether local cellular interactions were sufficient to give rise to global structural features of biofilms. Specifically, we asked whether chemorepulsion from a self-produced quorum-sensing molecule, autoinducer-2 (AI-2), was sufficient to recapitulate biofilm growth and cellular organization observed for biofilms of Helicobacter pylori, a common bacterial resident of human stomachs. To carry out this modeling, we modified an existing platform, Individual-based Dynamics of Microbial Communities Simulator (iDynoMiCS), to incorporate three-dimensional chemotaxis, planktonic cells that could join or leave the biofilm structure, and cellular production of AI-2. We simulated biofilm growth of previously characterized H. pylori strains with various AI-2 production and sensing capacities. Using biologically plausible parameters, we were able to recapitulate both the variation in biofilm mass and cellular distributions observed with these strains. Specifically, the strains that were competent to chemotax away from AI-2 produced smaller and more heterogeneously spaced biofilms, whereas the AI-2 chemotaxis-defective strains produced larger and more homogeneously spaced biofilms. The model also provided new insights into the cellular demographics contributing to the biofilm patterning of each strain. Our analysis supports the idea that cellular interactions at small spatial and temporal scales are sufficient to give rise to larger-scale emergent properties of biofilms. IMPORTANCE Most bacteria exist in aggregated, three-dimensional structures called biofilms. Although biofilms play important ecological roles in natural and engineered settings, they can also pose societal problems, for example, when they grow in plumbing systems or on medical implants. Understanding the processes that promote the growth and disassembly of biofilms could lead to better strategies to manage these structures. We had previously shown that Helicobacter pylori bacteria are repulsed by high concentrations of a self-produced molecule, AI-2, and that H. pylori mutants deficient in AI-2 sensing form larger and more homogeneously spaced biofilms. Here, we used computer simulations of biofilm formation to show that local H. pylori behavior of repulsion from high AI-2 could explain the overall architecture of H. pylori biofilms. Our findings demonstrate that it is possible to change global biofilm organization by manipulating local cell behaviors, which suggests that simple strategies targeting cells at local scales could be useful for controlling biofilms in industrial and medical settings.Emily G. SweeneyAndrew NishidaAlexandra WestonMaria S. BañuelosKristin PotterJohn ConeryKaren GuilleminAmerican Society for Microbiologyarticleautoinducer 2biofilmschemotaxiscomputer modelingMicrobiologyQR1-502ENmSphere, Vol 4, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	autoinducer 2 biofilms chemotaxis computer modeling Microbiology QR1-502
spellingShingle	autoinducer 2 biofilms chemotaxis computer modeling Microbiology QR1-502 Emily G. Sweeney Andrew Nishida Alexandra Weston Maria S. Bañuelos Kristin Potter John Conery Karen Guillemin Agent-Based Modeling Demonstrates How Local Chemotactic Behavior Can Shape Biofilm Architecture
description	ABSTRACT Bacteria are often found living in aggregated multicellular communities known as biofilms. Biofilms are three-dimensional structures that confer distinct physical and biological properties to the collective of cells living within them. We used agent-based modeling to explore whether local cellular interactions were sufficient to give rise to global structural features of biofilms. Specifically, we asked whether chemorepulsion from a self-produced quorum-sensing molecule, autoinducer-2 (AI-2), was sufficient to recapitulate biofilm growth and cellular organization observed for biofilms of Helicobacter pylori, a common bacterial resident of human stomachs. To carry out this modeling, we modified an existing platform, Individual-based Dynamics of Microbial Communities Simulator (iDynoMiCS), to incorporate three-dimensional chemotaxis, planktonic cells that could join or leave the biofilm structure, and cellular production of AI-2. We simulated biofilm growth of previously characterized H. pylori strains with various AI-2 production and sensing capacities. Using biologically plausible parameters, we were able to recapitulate both the variation in biofilm mass and cellular distributions observed with these strains. Specifically, the strains that were competent to chemotax away from AI-2 produced smaller and more heterogeneously spaced biofilms, whereas the AI-2 chemotaxis-defective strains produced larger and more homogeneously spaced biofilms. The model also provided new insights into the cellular demographics contributing to the biofilm patterning of each strain. Our analysis supports the idea that cellular interactions at small spatial and temporal scales are sufficient to give rise to larger-scale emergent properties of biofilms. IMPORTANCE Most bacteria exist in aggregated, three-dimensional structures called biofilms. Although biofilms play important ecological roles in natural and engineered settings, they can also pose societal problems, for example, when they grow in plumbing systems or on medical implants. Understanding the processes that promote the growth and disassembly of biofilms could lead to better strategies to manage these structures. We had previously shown that Helicobacter pylori bacteria are repulsed by high concentrations of a self-produced molecule, AI-2, and that H. pylori mutants deficient in AI-2 sensing form larger and more homogeneously spaced biofilms. Here, we used computer simulations of biofilm formation to show that local H. pylori behavior of repulsion from high AI-2 could explain the overall architecture of H. pylori biofilms. Our findings demonstrate that it is possible to change global biofilm organization by manipulating local cell behaviors, which suggests that simple strategies targeting cells at local scales could be useful for controlling biofilms in industrial and medical settings.
format	article
author	Emily G. Sweeney Andrew Nishida Alexandra Weston Maria S. Bañuelos Kristin Potter John Conery Karen Guillemin
author_facet	Emily G. Sweeney Andrew Nishida Alexandra Weston Maria S. Bañuelos Kristin Potter John Conery Karen Guillemin
author_sort	Emily G. Sweeney
title	Agent-Based Modeling Demonstrates How Local Chemotactic Behavior Can Shape Biofilm Architecture
title_short	Agent-Based Modeling Demonstrates How Local Chemotactic Behavior Can Shape Biofilm Architecture
title_full	Agent-Based Modeling Demonstrates How Local Chemotactic Behavior Can Shape Biofilm Architecture
title_fullStr	Agent-Based Modeling Demonstrates How Local Chemotactic Behavior Can Shape Biofilm Architecture
title_full_unstemmed	Agent-Based Modeling Demonstrates How Local Chemotactic Behavior Can Shape Biofilm Architecture
title_sort	agent-based modeling demonstrates how local chemotactic behavior can shape biofilm architecture
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/d3c261acaab04c50b6951dc6de6ec08f
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Agent-Based Modeling Demonstrates How Local Chemotactic Behavior Can Shape Biofilm Architecture

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