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Privatization of Biofilm Matrix in Structurally Heterogeneous Biofilms

Otto, Simon B. and Martin, Marivic and Schäfer, Daniel and Hartmann, Raimo and Drescher, Knut and Brix, Susanne and Dragoš, Anna and Kovács, Ákos T.. (2020) Privatization of Biofilm Matrix in Structurally Heterogeneous Biofilms. mSystems, 5 (4). e00425-20.

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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.
Faculties and Departments:05 Faculty of Science > Departement Biozentrum > Infection Biology > Microbiology and Biophysics (Drescher)
UniBasel Contributors:Drescher, Knut
Item Type:Article, refereed
Article Subtype:Research Article
Publisher:American Society for Microbiology
e-ISSN:2379-5077
Note:Publication type according to Uni Basel Research Database: Journal article
Language:English
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Last Modified:25 Jun 2021 09:06
Deposited On:25 Jun 2021 09:06

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