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Division of labor during biofilm matrix production

View ORCID ProfileAnna Dragoš, View ORCID ProfileHeiko Kiesewalter, View ORCID ProfileMarivic Martin, Chih-Yu Hsu, Raimo Hartmann, Tobias Wechsler, View ORCID ProfileKnut Drescher, View ORCID ProfileNicola Stanley-Wall, View ORCID ProfileRolf Kümmerli, View ORCID ProfileÁkos T. Kovács
doi: https://doi.org/10.1101/237230
Anna Dragoš
1Bacterial Interactions and Evolution Group, Department of Biotechnology and Biomedicine, Technical University of Denmark, Kgs Lyngby, 2800, Denmark
2Terrestrial Biofilms Group, Institute of Microbiology, Friedrich Schiller University Jena, Jena, 07743, Germany
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Heiko Kiesewalter
1Bacterial Interactions and Evolution Group, Department of Biotechnology and Biomedicine, Technical University of Denmark, Kgs Lyngby, 2800, Denmark
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Marivic Martin
1Bacterial Interactions and Evolution Group, Department of Biotechnology and Biomedicine, Technical University of Denmark, Kgs Lyngby, 2800, Denmark
2Terrestrial Biofilms Group, Institute of Microbiology, Friedrich Schiller University Jena, Jena, 07743, Germany
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Chih-Yu Hsu
3School of Life Sciences, University of Dundee, Dundee, DD1 5EH, United Kingdom
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Raimo Hartmann
4Max Planck Institute for Terrestrial Microbiology, Marburg, 35043, Germany
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Tobias Wechsler
5Department of Plant and Microbial Biology, University of Zürich, Zürich, 8057, Switzerland
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Knut Drescher
4Max Planck Institute for Terrestrial Microbiology, Marburg, 35043, Germany
6Department of Physics, Philipps University, Marburg, 35037, Germany
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Nicola Stanley-Wall
3School of Life Sciences, University of Dundee, Dundee, DD1 5EH, United Kingdom
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Rolf Kümmerli
5Department of Plant and Microbial Biology, University of Zürich, Zürich, 8057, Switzerland
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Ákos T. Kovács
1Bacterial Interactions and Evolution Group, Department of Biotechnology and Biomedicine, Technical University of Denmark, Kgs Lyngby, 2800, Denmark
2Terrestrial Biofilms Group, Institute of Microbiology, Friedrich Schiller University Jena, Jena, 07743, Germany
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Summary

Organisms as simple as bacteria can engage in complex collective actions, such as group motility and fruiting body formation. Some of these actions involve a division of labor, where phenotypically specialized clonal subpopulations, or genetically distinct lineages cooperate with each other by performing complementary tasks. Here, we combine experimental and computational approaches to investigate any benefits arising from division of labor during biofilm matrix production. We show that both phenotypic and genetic strategies for a division of labor can promote collective biofilm formation in the soil bacterium Bacillus subtilis. In this species, biofilm matrix consists of two major components; EPS and TasA. We observed that clonal groups of B. subtilis phenotypically segregate in three subpopulations composed of matrix non-producers, EPS-producers, and generalists, which produce both EPS and TasA. We further found that this incomplete phenotypic specialization was outperformed by a genetic division of labor, where two mutants, engineered as strict specialists, complemented each other by exchanging EPS and TasA. The relative fitness of the two mutants displayed a negative frequency dependence both in vitro and on plant roots, with strain frequency reaching an evolutionary stable equilibrium at 30% TasA-producers, corresponding exactly to the population composition where group fitness is maximized. Using individual-based modelling, we could show that asymmetries in strain ratio can arise due to differences in the relative benefits that matrix compounds generate for the collective; and that genetic division of labor can be favored when it breaks metabolic constraints associated with the simultaneous production of two matrix components.

Highlights

  • - matrix components EPS and TasA are costly public goods in B. subtilis biofilms

  • - genetic division of labor using Δeps and ΔtasA fosters maximal biofilm productivity

  • - Δeps and ΔtasA cooperation is evolutionary stable in laboratory and ecological systems

  • - costly metabolic coupling of public goods favors genetic division of labor

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted December 21, 2017.
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Division of labor during biofilm matrix production
Anna Dragoš, Heiko Kiesewalter, Marivic Martin, Chih-Yu Hsu, Raimo Hartmann, Tobias Wechsler, Knut Drescher, Nicola Stanley-Wall, Rolf Kümmerli, Ákos T. Kovács
bioRxiv 237230; doi: https://doi.org/10.1101/237230
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Division of labor during biofilm matrix production
Anna Dragoš, Heiko Kiesewalter, Marivic Martin, Chih-Yu Hsu, Raimo Hartmann, Tobias Wechsler, Knut Drescher, Nicola Stanley-Wall, Rolf Kümmerli, Ákos T. Kovács
bioRxiv 237230; doi: https://doi.org/10.1101/237230

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