Division of Labor during Biofilm Matrix Production

Anna Dragos, Heiko T. Kiesewalter, Marivic Martin, Chih Yu Hsu, Raimo Hartmann, Tobias Wechsler, Carsten Eriksen, Susanne Brix, Knut Drescher, Nicola Stanley-Wall, Rolf Kümmerli, Ákos T. Kovács*

*Corresponding author for this work

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Abstract

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 potential 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, exopolysaccharides (EPSs) and TasA. We observed that clonal groups of B. subtilis phenotypically segregate into three subpopulations composed of matrix non-producers, EPS producers, and generalists, which produce both EPSs and TasA. This incomplete phenotypic specialization was outperformed by a genetic division of labor, where two mutants, engineered as specialists, complemented each other by exchanging EPSs 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 a stable equilibrium at 30% TasA producers, corresponding exactly to the population composition where group productivity is maximized. Using individual-based modeling, we 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. Microbes that live predominantly in complex biofilms often cooperate with each other by performing complementary tasks. Dragoš et al. use a plant-colonizing Bacillus subtilis model and combine experimental and computational approaches to demonstrate and rationalize benefits arising from genetic division of labor during biofilm matrix production.
Original languageEnglish
JournalCurrent Biology
Volume28
Issue number12
Pages (from-to)1903-1913
ISSN0960-9822
DOIs
Publication statusPublished - 2018

Cite this

Dragos, Anna ; Kiesewalter, Heiko T. ; Martin, Marivic ; Hsu, Chih Yu ; Hartmann, Raimo ; Wechsler, Tobias ; Eriksen, Carsten ; Brix, Susanne ; Drescher, Knut ; Stanley-Wall, Nicola ; Kümmerli, Rolf ; Kovács, Ákos T. / Division of Labor during Biofilm Matrix Production. In: Current Biology. 2018 ; Vol. 28, No. 12. pp. 1903-1913.
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title = "Division of Labor during Biofilm Matrix Production",
abstract = "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 potential 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, exopolysaccharides (EPSs) and TasA. We observed that clonal groups of B. subtilis phenotypically segregate into three subpopulations composed of matrix non-producers, EPS producers, and generalists, which produce both EPSs and TasA. This incomplete phenotypic specialization was outperformed by a genetic division of labor, where two mutants, engineered as specialists, complemented each other by exchanging EPSs 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 a stable equilibrium at 30{\%} TasA producers, corresponding exactly to the population composition where group productivity is maximized. Using individual-based modeling, we 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. Microbes that live predominantly in complex biofilms often cooperate with each other by performing complementary tasks. Drago{\AA}¡ et al. use a plant-colonizing Bacillus subtilis model and combine experimental and computational approaches to demonstrate and rationalize benefits arising from genetic division of labor during biofilm matrix production.",
author = "Anna Dragos and Kiesewalter, {Heiko T.} and Marivic Martin and Hsu, {Chih Yu} and Raimo Hartmann and Tobias Wechsler and Carsten Eriksen and Susanne Brix and Knut Drescher and Nicola Stanley-Wall and Rolf K{\"u}mmerli and Kov{\'a}cs, {{\'A}kos T.}",
year = "2018",
doi = "10.1016/j.cub.2018.04.046",
language = "English",
volume = "28",
pages = "1903--1913",
journal = "Current Biology",
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Dragos, A, Kiesewalter, HT, Martin, M, Hsu, CY, Hartmann, R, Wechsler, T, Eriksen, C, Brix, S, Drescher, K, Stanley-Wall, N, Kümmerli, R & Kovács, ÁT 2018, 'Division of Labor during Biofilm Matrix Production', Current Biology, vol. 28, no. 12, pp. 1903-1913. https://doi.org/10.1016/j.cub.2018.04.046

Division of Labor during Biofilm Matrix Production. / Dragos, Anna; Kiesewalter, Heiko T.; Martin, Marivic; Hsu, Chih Yu; Hartmann, Raimo; Wechsler, Tobias; Eriksen, Carsten; Brix, Susanne; Drescher, Knut; Stanley-Wall, Nicola; Kümmerli, Rolf; Kovács, Ákos T.

In: Current Biology, Vol. 28, No. 12, 2018, p. 1903-1913.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Division of Labor during Biofilm Matrix Production

AU - Dragos, Anna

AU - Kiesewalter, Heiko T.

AU - Martin, Marivic

AU - Hsu, Chih Yu

AU - Hartmann, Raimo

AU - Wechsler, Tobias

AU - Eriksen, Carsten

AU - Brix, Susanne

AU - Drescher, Knut

AU - Stanley-Wall, Nicola

AU - Kümmerli, Rolf

AU - Kovács, Ákos T.

PY - 2018

Y1 - 2018

N2 - 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 potential 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, exopolysaccharides (EPSs) and TasA. We observed that clonal groups of B. subtilis phenotypically segregate into three subpopulations composed of matrix non-producers, EPS producers, and generalists, which produce both EPSs and TasA. This incomplete phenotypic specialization was outperformed by a genetic division of labor, where two mutants, engineered as specialists, complemented each other by exchanging EPSs 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 a stable equilibrium at 30% TasA producers, corresponding exactly to the population composition where group productivity is maximized. Using individual-based modeling, we 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. Microbes that live predominantly in complex biofilms often cooperate with each other by performing complementary tasks. Dragoš et al. use a plant-colonizing Bacillus subtilis model and combine experimental and computational approaches to demonstrate and rationalize benefits arising from genetic division of labor during biofilm matrix production.

AB - 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 potential 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, exopolysaccharides (EPSs) and TasA. We observed that clonal groups of B. subtilis phenotypically segregate into three subpopulations composed of matrix non-producers, EPS producers, and generalists, which produce both EPSs and TasA. This incomplete phenotypic specialization was outperformed by a genetic division of labor, where two mutants, engineered as specialists, complemented each other by exchanging EPSs 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 a stable equilibrium at 30% TasA producers, corresponding exactly to the population composition where group productivity is maximized. Using individual-based modeling, we 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. Microbes that live predominantly in complex biofilms often cooperate with each other by performing complementary tasks. Dragoš et al. use a plant-colonizing Bacillus subtilis model and combine experimental and computational approaches to demonstrate and rationalize benefits arising from genetic division of labor during biofilm matrix production.

U2 - 10.1016/j.cub.2018.04.046

DO - 10.1016/j.cub.2018.04.046

M3 - Journal article

VL - 28

SP - 1903

EP - 1913

JO - Current Biology

JF - Current Biology

SN - 0960-9822

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ER -