Phenotypic Heterogeneity in Bacterial Quorum Sensing Systems

Bettenworth, Vera; Steinfeld, Benedikt; Duin, Hilke; Petersen, Katrin; Streit, Wolfgang R.; Bischofs, Ilka B.; Becker, Anke

doi:10.1016/j.jmb.2019.04.036

Cited by 55 publications

(52 citation statements)

References 158 publications

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“…There are several potential input signals, which may contribute to heterogeneous sporulation [80] and the division of labor in biofilms [81]. How a QS system in general and ComX in particular mechanistically contribute to the heterogeneity of gene expression is not yet understood [45]. We speculate that ComX informs the population on its growth rate and may act as a gatekeeper, which allows investments into late growth adaptations only when growth slows down.…”

Section: Discussionmentioning

confidence: 98%

“…Cells resident in biofilms simultaneously express multiple biological states and this phenotypic heterogeneity results, for example, in the coexistence of matrix producers and highly resistant spores in one biofilm [9,24,44]. QS often regulates adaptive traits that exhibit phenotypic heterogeneity in many different species [45]. However, how ComX density-dependent communication affects the distribution of biological states devoted to the production of matrix components or sporulation in the pellicle biofilm, is less understood.…”

Section: Introductionmentioning

confidence: 99%

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The ComX Quorum Sensing Peptide of Bacillus subtilis Affects Biofilm Formation Negatively and Sporulation Positively

et al. 2020

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Quorum sensing (QS) is often required for the formation of bacterial biofilms and is a popular target of biofilm control strategies. Previous studies implicate the ComQXPA quorum sensing system of Bacillus subtilis as a promoter of biofilm formation. Here, we report that ComX signaling peptide deficient mutants form thicker and more robust pellicle biofilms that contain chains of cells. We confirm that ComX positively affects the transcriptional activity of the PepsA promoter, which controls the synthesis of the major matrix polysaccharide. In contrast, ComX negatively controls the PtapA promoter, which drives the production of TasA, a fibrous matrix protein. Overall, the biomass of the mutant biofilm lacking ComX accumulates more monosaccharide and protein content than the wild type. We conclude that this QS phenotype might be due to extended investment into growth rather than spore development. Consistent with this, the ComX deficient mutant shows a delayed activation of the pre-spore specific promoter, PspoIIQ, and a delayed, more synchronous commitment to sporulation. We conclude that ComX mediated early commitment to sporulation of the wild type slows down biofilm formation and modulates the coexistence of multiple biological states during the early stages of biofilm development.

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Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

The ComX Quorum Sensing Peptide of Bacillus subtilis Affects Biofilm Formation Negatively and Sporulation Positively

et al. 2020

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“…The rapA-phrA operon is highly regulated [27][28][29][30][31][32] and is activated under both non-sporulating 30,31 and sporulating 16,27,28,33 conditions, indicating that signaling takes place in different situations. Interestingly, under some conditions the operon is expressed heterogeneously across the population 18 (a phenomenon that has been observed for other rap-phr-signaling systems 16 ), which might point at a signaling function beyond classical quorum sensing 34 . Specifically, in a heterogeneous population its composition might be a relevant parameter for cellular decision-making.…”

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confidence: 75%

Ratiometric population sensing by a pump-probe signaling system in Bacillus subtilis

et al. 2020

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Communication by means of diffusible signaling molecules facilitates higher-level organization of cellular populations. Gram-positive bacteria frequently use signaling peptides, which are either detected at the cell surface or 'probed' by intracellular receptors after being pumped into the cytoplasm. While the former type is used to monitor cell density, the functions of pump-probe networks are less clear. Here we show that pump-probe networks can, in principle, perform different tasks and mediate quorum-sensing, chronometric and ratiometric control. We characterize the properties of the prototypical PhrA-RapA system in Bacillus subtilis using FRET. We find that changes in extracellular PhrA concentrations are tracked rather poorly; instead, cells accumulate and strongly amplify the signal in a dosedependent manner. This suggests that the PhrA-RapA system, and others like it, have evolved to sense changes in the composition of heterogeneous populations and infer the fraction of signal-producing cells in a mixed population to coordinate cellular behaviors.

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“…systems. Much like colonies of the clonal raider ant, these systems exhibit patterns that can be interpreted as behavioral convergence (60–64), divergence (65), and non-linear effects of mixing on group-level phenotypes (66–68). In turn, these patterns affect important processes such as collective decision-making (5), the transmission and evolution of disease (69, 70), and the evolution of cooperative behavior (71, 72).…”

Section: Discussionmentioning

confidence: 99%

Emergent behavioral organization in heterogeneous groups of a social insect

Ulrich

Kawakatsu²,

Tokita

et al. 2020

Preprint

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The composition of social groups has profound effects on their function, from collective decision-making to foraging efficiency. But few social systems afford sufficient control over group composition to precisely quantify its effects on individual and collective behavior. Here we combine experimental and theoretical approaches to study the effect of group composition on individual behavior and division of labor (DOL) in a social insect. Experimentally, we use automated behavioral tracking to monitor 120 colonies of the clonal raider ant, Ooceraea biroi, with controlled variation in three key correlates of social insect behavior: genotype, age, and morphology. We find that each of these sources of heterogeneity generates a distinct pattern of behavioral organization, including the amplification or dampening of inherent behavioral differences in colonies with mixed types. Theoretically, we use a well-studied model of DOL to explore potential mechanisms underlying the experimental findings. We find that the simplest implementation of this model, which assumes that heterogeneous individuals differ only in response thresholds, could only partially recapitulate the empirically observed patterns of behavior. However, the full spectrum of observed phenomena was recapitulated by extending the model to incorporate two factors that are biologically meaningful but theoretically rarely considered: variation among workers in task performance efficiency and among larvae in task demand. Our results thus show that different sources of heterogeneity within social groups can generate different, sometimes non-intuitive, behavioral effects, but that relatively simple models can capture these dynamics and thereby begin to elucidate the basic organizational principles of DOL in social insects.Significance StatementWhen individuals interact in an aggregate, many factors that are not known a priori affect group dynamics. A social group will therefore show emergent properties that cannot easily be predicted from how its members behave in isolation. This problem is exacerbated in mixed groups, where different individuals have different behavioral tendencies. Here we describe different facets of collective behavioral organization in mixed groups of the clonal raider ant, and show that a simple theoretical model can capture even non-intuitive aspects of the behavioral data. These results begin to reveal the principles underlying emergent behavioral organization in social insects. Importantly, our insights might apply to complex biological systems more generally and be used to help engineer collective behavior in artificial systems.

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Phenotypic Heterogeneity in Bacterial Quorum Sensing Systems

Cited by 55 publications

References 158 publications

The ComX Quorum Sensing Peptide of Bacillus subtilis Affects Biofilm Formation Negatively and Sporulation Positively

The ComX Quorum Sensing Peptide of Bacillus subtilis Affects Biofilm Formation Negatively and Sporulation Positively

Ratiometric population sensing by a pump-probe signaling system in Bacillus subtilis

Emergent behavioral organization in heterogeneous groups of a social insect

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