Privatization of Biofilm Matrix in Structurally Heterogeneous Biofilms

ABSTRACT The self-produced biofilm provides beneficial protection for the enclosed cells, but the costly production of matrix components makes producer cells susceptible to cheating by nonproducing individuals. Despite detrimental effects of nonproducers, biofilms can be heterogeneous, with isogenic...

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Autores principales:	Simon B. Otto, Marivic Martin, Daniel Schäfer, Raimo Hartmann, Knut Drescher, Susanne Brix, Anna Dragoš, Ákos T. Kovács
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Bacillus subtilis biofilm phenotypic heterogeneity structural heterogeneity exopolysaccharide Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d00adb5b586f4bb2a92eeb23bfb31e90
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spelling	oai:doaj.org-article:d00adb5b586f4bb2a92eeb23bfb31e902021-12-02T19:47:38ZPrivatization of Biofilm Matrix in Structurally Heterogeneous Biofilms10.1128/mSystems.00425-202379-5077https://doaj.org/article/d00adb5b586f4bb2a92eeb23bfb31e902020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00425-20https://doaj.org/toc/2379-5077ABSTRACT The self-produced biofilm provides beneficial protection for the enclosed cells, but the costly production of matrix components makes producer cells susceptible to cheating by nonproducing individuals. Despite detrimental effects of nonproducers, biofilms can be heterogeneous, with isogenic nonproducers being a natural consequence of phenotypic differentiation processes. For instance, in Bacillus subtilis biofilm cells differ in production of the two major matrix components, the amyloid fiber protein TasA and exopolysaccharides (EPS), demonstrating different expression levels of corresponding matrix genes. This raises questions regarding matrix gene expression dynamics during biofilm development and the impact of phenotypic nonproducers on biofilm robustness. Here, we show that biofilms are structurally heterogeneous and can be separated into strongly and weakly associated clusters. We reveal that spatiotemporal changes in structural heterogeneity correlate with matrix gene expression, with TasA playing a key role in biofilm integrity and timing of development. We show that the matrix remains partially privatized by the producer subpopulation, where cells tightly stick together even when exposed to shear stress. Our results support previous findings on the existence of “weak points” in seemingly robust biofilms as well as on the key role of linkage proteins in biofilm formation. Furthermore, we provide a starting point for investigating the privatization of common goods within isogenic populations. IMPORTANCE Biofilms are communities of bacteria protected by a self-produced extracellular matrix. The detrimental effects of nonproducing individuals on biofilm development raise questions about the dynamics between community members, especially when isogenic nonproducers exist within wild-type populations. We asked ourselves whether phenotypic nonproducers impact biofilm robustness, and where and when this heterogeneity of matrix gene expression occurs. Based on our results, we propose that the matrix remains partly privatized by the producing subpopulation, since producing cells stick together when exposed to shear stress. The important role of linkage proteins in robustness and development of the structurally heterogeneous biofilm provides an entry into studying the privatization of common goods within isogenic populations.Simon B. OttoMarivic MartinDaniel SchäferRaimo HartmannKnut DrescherSusanne BrixAnna DragošÁkos T. KovácsAmerican Society for MicrobiologyarticleBacillus subtilisbiofilmphenotypic heterogeneitystructural heterogeneityexopolysaccharideMicrobiologyQR1-502ENmSystems, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacillus subtilis biofilm phenotypic heterogeneity structural heterogeneity exopolysaccharide Microbiology QR1-502
spellingShingle	Bacillus subtilis biofilm phenotypic heterogeneity structural heterogeneity exopolysaccharide Microbiology QR1-502 Simon B. Otto Marivic Martin Daniel Schäfer Raimo Hartmann Knut Drescher Susanne Brix Anna Dragoš Ákos T. Kovács Privatization of Biofilm Matrix in Structurally Heterogeneous Biofilms
description	ABSTRACT The self-produced biofilm provides beneficial protection for the enclosed cells, but the costly production of matrix components makes producer cells susceptible to cheating by nonproducing individuals. Despite detrimental effects of nonproducers, biofilms can be heterogeneous, with isogenic nonproducers being a natural consequence of phenotypic differentiation processes. For instance, in Bacillus subtilis biofilm cells differ in production of the two major matrix components, the amyloid fiber protein TasA and exopolysaccharides (EPS), demonstrating different expression levels of corresponding matrix genes. This raises questions regarding matrix gene expression dynamics during biofilm development and the impact of phenotypic nonproducers on biofilm robustness. Here, we show that biofilms are structurally heterogeneous and can be separated into strongly and weakly associated clusters. We reveal that spatiotemporal changes in structural heterogeneity correlate with matrix gene expression, with TasA playing a key role in biofilm integrity and timing of development. We show that the matrix remains partially privatized by the producer subpopulation, where cells tightly stick together even when exposed to shear stress. Our results support previous findings on the existence of “weak points” in seemingly robust biofilms as well as on the key role of linkage proteins in biofilm formation. Furthermore, we provide a starting point for investigating the privatization of common goods within isogenic populations. IMPORTANCE Biofilms are communities of bacteria protected by a self-produced extracellular matrix. The detrimental effects of nonproducing individuals on biofilm development raise questions about the dynamics between community members, especially when isogenic nonproducers exist within wild-type populations. We asked ourselves whether phenotypic nonproducers impact biofilm robustness, and where and when this heterogeneity of matrix gene expression occurs. Based on our results, we propose that the matrix remains partly privatized by the producing subpopulation, since producing cells stick together when exposed to shear stress. The important role of linkage proteins in robustness and development of the structurally heterogeneous biofilm provides an entry into studying the privatization of common goods within isogenic populations.
format	article
author	Simon B. Otto Marivic Martin Daniel Schäfer Raimo Hartmann Knut Drescher Susanne Brix Anna Dragoš Ákos T. Kovács
author_facet	Simon B. Otto Marivic Martin Daniel Schäfer Raimo Hartmann Knut Drescher Susanne Brix Anna Dragoš Ákos T. Kovács
author_sort	Simon B. Otto
title	Privatization of Biofilm Matrix in Structurally Heterogeneous Biofilms
title_short	Privatization of Biofilm Matrix in Structurally Heterogeneous Biofilms
title_full	Privatization of Biofilm Matrix in Structurally Heterogeneous Biofilms
title_fullStr	Privatization of Biofilm Matrix in Structurally Heterogeneous Biofilms
title_full_unstemmed	Privatization of Biofilm Matrix in Structurally Heterogeneous Biofilms
title_sort	privatization of biofilm matrix in structurally heterogeneous biofilms
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/d00adb5b586f4bb2a92eeb23bfb31e90
work_keys_str_mv	AT simonbotto privatizationofbiofilmmatrixinstructurallyheterogeneousbiofilms AT marivicmartin privatizationofbiofilmmatrixinstructurallyheterogeneousbiofilms AT danielschafer privatizationofbiofilmmatrixinstructurallyheterogeneousbiofilms AT raimohartmann privatizationofbiofilmmatrixinstructurallyheterogeneousbiofilms AT knutdrescher privatizationofbiofilmmatrixinstructurallyheterogeneousbiofilms AT susannebrix privatizationofbiofilmmatrixinstructurallyheterogeneousbiofilms AT annadragos privatizationofbiofilmmatrixinstructurallyheterogeneousbiofilms AT akostkovacs privatizationofbiofilmmatrixinstructurallyheterogeneousbiofilms
_version_	1718375990779969536

Privatization of Biofilm Matrix in Structurally Heterogeneous Biofilms

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