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Research Article | Ecological and Evolutionary Science

Privatization of Biofilm Matrix in Structurally Heterogeneous Biofilms

Simon B. Otto, Marivic Martin, Daniel Schäfer, Raimo Hartmann, Knut Drescher, Susanne Brix, Anna Dragoš, Ákos T. Kovács
Mark J. Mandel, Editor
Simon B. Otto
aBacterial Interactions and Evolution Group, Department of Biotechnology and Biomedicine, Technical University of Denmark, Kongens Lyngby, Denmark
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Marivic Martin
aBacterial Interactions and Evolution Group, Department of Biotechnology and Biomedicine, Technical University of Denmark, Kongens Lyngby, Denmark
bTerrestrial Biofilms Group, Institute of Microbiology, Friedrich Schiller University Jena, Jena, Germany
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Daniel Schäfer
bTerrestrial Biofilms Group, Institute of Microbiology, Friedrich Schiller University Jena, Jena, Germany
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Raimo Hartmann
cMax Planck Institute for Terrestrial Microbiology, Marburg, Germany
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Knut Drescher
cMax Planck Institute for Terrestrial Microbiology, Marburg, Germany
dDepartment of Physics, Philipps-Universität Marburg, Marburg, Germany
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Susanne Brix
eDisease Systems Immunology Group, Department of Biotechnology and Biomedicine, Technical University of Denmark, Kongens Lyngby, Denmark
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Anna Dragoš
aBacterial Interactions and Evolution Group, Department of Biotechnology and Biomedicine, Technical University of Denmark, Kongens Lyngby, Denmark
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Ákos T. Kovács
aBacterial Interactions and Evolution Group, Department of Biotechnology and Biomedicine, Technical University of Denmark, Kongens Lyngby, Denmark
bTerrestrial Biofilms Group, Institute of Microbiology, Friedrich Schiller University Jena, Jena, Germany
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Mark J. Mandel
University of Wisconsin-Madison
Roles: Editor
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Yunrong Chai
Northeastern University
Roles: ad hoc peer reviewer
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DOI: 10.1128/mSystems.00425-20
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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.

FOOTNOTES

    • Received May 11, 2020.
    • Accepted July 13, 2020.
  • The review history of this article can be read here.

  • Copyright © 2020 Otto et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Privatization of Biofilm Matrix in Structurally Heterogeneous Biofilms
Simon B. Otto, Marivic Martin, Daniel Schäfer, Raimo Hartmann, Knut Drescher, Susanne Brix, Anna Dragoš, Ákos T. Kovács
mSystems Aug 2020, 5 (4) e00425-20; DOI: 10.1128/mSystems.00425-20

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Privatization of Biofilm Matrix in Structurally Heterogeneous Biofilms
Simon B. Otto, Marivic Martin, Daniel Schäfer, Raimo Hartmann, Knut Drescher, Susanne Brix, Anna Dragoš, Ákos T. Kovács
mSystems Aug 2020, 5 (4) e00425-20; DOI: 10.1128/mSystems.00425-20
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KEYWORDS

Bacillus subtilis
biofilm
phenotypic heterogeneity
structural heterogeneity
exopolysaccharide

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