Extracellular Polymeric Substance Production and Aggregated Bacteria Colonization Influence the Competition of Microbes in Biofilms

The production of extracellular polymeric substance (EPS) is important for the survival of biofilms. However, EPS production is costly for bacteria and the bacterial strains that produce EPS (EPS+) grow in the same environment as non-producers (EPS−) leading to competition between these strains for...

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Main Authors: Pahala G. Jayathilake, Saikat Jana, Steve Rushton, David Swailes, Ben Bridgens, Tom Curtis, Jinju Chen
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-09-01
Series:Frontiers in Microbiology
Subjects:
EPS
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.01865/full
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spelling doaj-e0b21063ba2448729107e8d27acd01082020-11-24T22:10:44ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-09-01810.3389/fmicb.2017.01865277189Extracellular Polymeric Substance Production and Aggregated Bacteria Colonization Influence the Competition of Microbes in BiofilmsPahala G. Jayathilake0Saikat Jana1Steve Rushton2David Swailes3Ben Bridgens4Tom Curtis5Jinju Chen6School of Engineering, Newcastle University, Newcastle upon Tyne, United KingdomSchool of Engineering, Newcastle University, Newcastle upon Tyne, United KingdomSchool of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, United KingdomSchool of Mathematics, Statistics and Physics, Newcastle University, Newcastle upon Tyne, United KingdomSchool of Engineering, Newcastle University, Newcastle upon Tyne, United KingdomCentre for Synthetic Biology and the Bioeconomy, Newcastle University, Newcastle upon Tyne, United KingdomSchool of Engineering, Newcastle University, Newcastle upon Tyne, United KingdomThe production of extracellular polymeric substance (EPS) is important for the survival of biofilms. However, EPS production is costly for bacteria and the bacterial strains that produce EPS (EPS+) grow in the same environment as non-producers (EPS−) leading to competition between these strains for nutrients and space. The outcome of this competition is likely to be dependent on factors such as initial attachment, EPS production rate, ambient nutrient levels and quorum sensing. We use an Individual-based Model (IbM) to study the competition between EPS+ and EPS− strains by varying the nature of initial colonizers which can either be in the form of single cells or multicellular aggregates. The microbes with EPS+ characteristics obtain a competitive advantage if they initially colonize the surface as smaller aggregates and are widely spread-out between the cells of EPS−, when both are deposited on the substratum. Furthermore, the results show that quorum sensing-regulated EPS production may significantly reduce the fitness of EPS producers when they initially deposit as aggregates. The results provide insights into how the distribution of bacterial aggregates during initial colonization could be a deciding factor in the competition among different strains in biofilms.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01865/fullindividual-based modelbiofilmcompetitionEPSaggregatesquorum sensing
collection DOAJ
language English
format Article
sources DOAJ
author Pahala G. Jayathilake
Saikat Jana
Steve Rushton
David Swailes
Ben Bridgens
Tom Curtis
Jinju Chen
spellingShingle Pahala G. Jayathilake
Saikat Jana
Steve Rushton
David Swailes
Ben Bridgens
Tom Curtis
Jinju Chen
Extracellular Polymeric Substance Production and Aggregated Bacteria Colonization Influence the Competition of Microbes in Biofilms
Frontiers in Microbiology
individual-based model
biofilm
competition
EPS
aggregates
quorum sensing
author_facet Pahala G. Jayathilake
Saikat Jana
Steve Rushton
David Swailes
Ben Bridgens
Tom Curtis
Jinju Chen
author_sort Pahala G. Jayathilake
title Extracellular Polymeric Substance Production and Aggregated Bacteria Colonization Influence the Competition of Microbes in Biofilms
title_short Extracellular Polymeric Substance Production and Aggregated Bacteria Colonization Influence the Competition of Microbes in Biofilms
title_full Extracellular Polymeric Substance Production and Aggregated Bacteria Colonization Influence the Competition of Microbes in Biofilms
title_fullStr Extracellular Polymeric Substance Production and Aggregated Bacteria Colonization Influence the Competition of Microbes in Biofilms
title_full_unstemmed Extracellular Polymeric Substance Production and Aggregated Bacteria Colonization Influence the Competition of Microbes in Biofilms
title_sort extracellular polymeric substance production and aggregated bacteria colonization influence the competition of microbes in biofilms
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2017-09-01
description The production of extracellular polymeric substance (EPS) is important for the survival of biofilms. However, EPS production is costly for bacteria and the bacterial strains that produce EPS (EPS+) grow in the same environment as non-producers (EPS−) leading to competition between these strains for nutrients and space. The outcome of this competition is likely to be dependent on factors such as initial attachment, EPS production rate, ambient nutrient levels and quorum sensing. We use an Individual-based Model (IbM) to study the competition between EPS+ and EPS− strains by varying the nature of initial colonizers which can either be in the form of single cells or multicellular aggregates. The microbes with EPS+ characteristics obtain a competitive advantage if they initially colonize the surface as smaller aggregates and are widely spread-out between the cells of EPS−, when both are deposited on the substratum. Furthermore, the results show that quorum sensing-regulated EPS production may significantly reduce the fitness of EPS producers when they initially deposit as aggregates. The results provide insights into how the distribution of bacterial aggregates during initial colonization could be a deciding factor in the competition among different strains in biofilms.
topic individual-based model
biofilm
competition
EPS
aggregates
quorum sensing
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.01865/full
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