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Simulation of Escherichia coli Dynamics in Biofilms and Submerged Colonies with an Individual-Based Model Including Metabolic Network Information

Clustered microbial communities are omnipresent in the food industry, e.g., as colonies of microbial pathogens in/on food media or as biofilms on food processing surfaces. These clustered communities are often characterized by metabolic differentiation among their constituting cells as a result of h...

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Autores principales: Tack, Ignace L. M. M., Nimmegeers, Philippe, Akkermans, Simen, Hashem, Ihab, Van Impe, Jan F. M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5733555/
https://www.ncbi.nlm.nih.gov/pubmed/29321772
http://dx.doi.org/10.3389/fmicb.2017.02509
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author Tack, Ignace L. M. M.
Nimmegeers, Philippe
Akkermans, Simen
Hashem, Ihab
Van Impe, Jan F. M.
author_facet Tack, Ignace L. M. M.
Nimmegeers, Philippe
Akkermans, Simen
Hashem, Ihab
Van Impe, Jan F. M.
author_sort Tack, Ignace L. M. M.
collection PubMed
description Clustered microbial communities are omnipresent in the food industry, e.g., as colonies of microbial pathogens in/on food media or as biofilms on food processing surfaces. These clustered communities are often characterized by metabolic differentiation among their constituting cells as a result of heterogeneous environmental conditions in the cellular surroundings. This paper focuses on the role of metabolic differentiation due to oxygen gradients in the development of Escherichia coli cell communities, whereby low local oxygen concentrations lead to cellular secretion of weak acid products. For this reason, a metabolic model has been developed for the facultative anaerobe E. coli covering the range of aerobic, microaerobic, and anaerobic environmental conditions. This metabolic model is expressed as a multiparametric programming problem, in which the influence of low extracellular pH values and the presence of undissociated acid cell products in the environment has been taken into account. Furthermore, the developed metabolic model is incorporated in MICRODIMS, an in-house developed individual-based modeling framework to simulate microbial colony and biofilm dynamics. Two case studies have been elaborated using the MICRODIMS simulator: (i) biofilm growth on a substratum surface and (ii) submerged colony growth in a semi-solid mixed food product. In the first case study, the acidification of the biofilm environment and the emergence of typical biofilm morphologies have been observed, such as the mushroom-shaped structure of mature biofilms and the formation of cellular chains at the exterior surface of the biofilm. The simulations show that these morphological phenomena are respectively dependent on the initial affinity of pioneer cells for the substratum surface and the cell detachment process at the outer surface of the biofilm. In the second case study, a no-growth zone emerges in the colony center due to a local decline of the environmental pH. As a result, cellular growth in the submerged colony is limited to the colony periphery, implying a linear increase of the colony radius over time. MICRODIMS has been successfully used to reproduce complex dynamics of clustered microbial communities.
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spelling pubmed-57335552018-01-10 Simulation of Escherichia coli Dynamics in Biofilms and Submerged Colonies with an Individual-Based Model Including Metabolic Network Information Tack, Ignace L. M. M. Nimmegeers, Philippe Akkermans, Simen Hashem, Ihab Van Impe, Jan F. M. Front Microbiol Microbiology Clustered microbial communities are omnipresent in the food industry, e.g., as colonies of microbial pathogens in/on food media or as biofilms on food processing surfaces. These clustered communities are often characterized by metabolic differentiation among their constituting cells as a result of heterogeneous environmental conditions in the cellular surroundings. This paper focuses on the role of metabolic differentiation due to oxygen gradients in the development of Escherichia coli cell communities, whereby low local oxygen concentrations lead to cellular secretion of weak acid products. For this reason, a metabolic model has been developed for the facultative anaerobe E. coli covering the range of aerobic, microaerobic, and anaerobic environmental conditions. This metabolic model is expressed as a multiparametric programming problem, in which the influence of low extracellular pH values and the presence of undissociated acid cell products in the environment has been taken into account. Furthermore, the developed metabolic model is incorporated in MICRODIMS, an in-house developed individual-based modeling framework to simulate microbial colony and biofilm dynamics. Two case studies have been elaborated using the MICRODIMS simulator: (i) biofilm growth on a substratum surface and (ii) submerged colony growth in a semi-solid mixed food product. In the first case study, the acidification of the biofilm environment and the emergence of typical biofilm morphologies have been observed, such as the mushroom-shaped structure of mature biofilms and the formation of cellular chains at the exterior surface of the biofilm. The simulations show that these morphological phenomena are respectively dependent on the initial affinity of pioneer cells for the substratum surface and the cell detachment process at the outer surface of the biofilm. In the second case study, a no-growth zone emerges in the colony center due to a local decline of the environmental pH. As a result, cellular growth in the submerged colony is limited to the colony periphery, implying a linear increase of the colony radius over time. MICRODIMS has been successfully used to reproduce complex dynamics of clustered microbial communities. Frontiers Media S.A. 2017-12-13 /pmc/articles/PMC5733555/ /pubmed/29321772 http://dx.doi.org/10.3389/fmicb.2017.02509 Text en Copyright © 2017 Tack, Nimmegeers, Akkermans, Hashem and Van Impe. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Tack, Ignace L. M. M.
Nimmegeers, Philippe
Akkermans, Simen
Hashem, Ihab
Van Impe, Jan F. M.
Simulation of Escherichia coli Dynamics in Biofilms and Submerged Colonies with an Individual-Based Model Including Metabolic Network Information
title Simulation of Escherichia coli Dynamics in Biofilms and Submerged Colonies with an Individual-Based Model Including Metabolic Network Information
title_full Simulation of Escherichia coli Dynamics in Biofilms and Submerged Colonies with an Individual-Based Model Including Metabolic Network Information
title_fullStr Simulation of Escherichia coli Dynamics in Biofilms and Submerged Colonies with an Individual-Based Model Including Metabolic Network Information
title_full_unstemmed Simulation of Escherichia coli Dynamics in Biofilms and Submerged Colonies with an Individual-Based Model Including Metabolic Network Information
title_short Simulation of Escherichia coli Dynamics in Biofilms and Submerged Colonies with an Individual-Based Model Including Metabolic Network Information
title_sort simulation of escherichia coli dynamics in biofilms and submerged colonies with an individual-based model including metabolic network information
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5733555/
https://www.ncbi.nlm.nih.gov/pubmed/29321772
http://dx.doi.org/10.3389/fmicb.2017.02509
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