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

Research output: Contribution to journalJournal articleResearchpeer-review

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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

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