Dataset Information

Vibrio cholerae Combines Individual and Collective Sensing to Trigger Biofilm Dispersal.

ABSTRACT: Bacteria can generate benefits for themselves and their kin by living in multicellular, matrix-enclosed communities, termed biofilms, which are fundamental to microbial ecology and the impact bacteria have on the environment, infections, and industry [1-6]. The advantages of the biofilm mode of life include increased stress resistance and access to concentrated nutrient sources [3, 7, 8]. However, there are also costs associated with biofilm growth, including the metabolic burden of biofilm matrix production, increased resource competition, and limited mobility inside the community [9-11]. The decision-making strategies used by bacteria to weigh the costs between remaining in a biofilm or actively dispersing are largely unclear, even though the dispersal transition is a central aspect of the biofilm life cycle and critical for infection transmission [12-14]. Using a combination of genetic and novel single-cell imaging approaches, we show that Vibrio cholerae integrates dual sensory inputs to control the dispersal response: cells use the general stress response, which can be induced via starvation, and they also integrate information about the local cell density and molecular transport conditions in the environment via the quorum sensing apparatus. By combining information from individual (stress response) and collective (quorum sensing) avenues of sensory input, biofilm-dwelling bacteria can make robust decisions to disperse from large biofilms under distress, while preventing premature dispersal when biofilm populations are small. These insights into triggers and regulators of biofilm dispersal are a key step toward actively inducing biofilm dispersal for technological and medical applications, and for environmental control of biofilms.

SUBMITTER: Singh PK

PROVIDER: S-EPMC5678073 | biostudies-literature | 2017 Nov

REPOSITORIES: biostudies-literature

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Vibrio cholerae Combines Individual and Collective Sensing to Trigger Biofilm Dispersal.

Singh Praveen K PK Bartalomej Sabina S Hartmann Raimo R Jeckel Hannah H Vidakovic Lucia L Nadell Carey D CD Drescher Knut K

Current biology : CB 20171019 21

Bacteria can generate benefits for themselves and their kin by living in multicellular, matrix-enclosed communities, termed biofilms, which are fundamental to microbial ecology and the impact bacteria have on the environment, infections, and industry [1-6]. The advantages of the biofilm mode of life include increased stress resistance and access to concentrated nutrient sources [3, 7, 8]. However, there are also costs associated with biofilm growth, including the metabolic burden of biofilm matr ...[more]

PMID: 29056457

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Project description:Vibrio cholerae possesses multiple quorum-sensing (QS) systems that control virulence and biofilm formation among other traits. At low cell densities, when QS autoinducers are absent, V. cholerae forms biofilms. At high cell densities, when autoinducers have accumulated, biofilm formation is repressed, and dispersal occurs. Here, we focus on the roles of two well-characterized QS autoinducers that function in parallel. One autoinducer, called cholerae autoinducer-1 (CAI-1), is used to measure Vibrio abundance, and the other autoinducer, called autoinducer-2 (AI-2), is widely produced by different bacterial species and presumed to enable V. cholerae to assess the total bacterial cell density of the vicinal community. The two V. cholerae autoinducers funnel information into a shared signal relay pathway. This feature of the QS system architecture has made it difficult to understand how specific information can be extracted from each autoinducer, how the autoinducers might drive distinct output behaviors, and, in turn, how the bacteria use QS to distinguish kin from nonkin in bacterial communities. We develop a live-cell biofilm formation and dispersal assay that allows examination of the individual and combined roles of the two autoinducers in controlling V. cholerae behavior. We show that the QS system works as a coincidence detector in which both autoinducers must be present simultaneously for repression of biofilm formation to occur. Within that context, the CAI-1 QS pathway is activated when only a few V. cholerae cells are present, whereas the AI-2 pathway is activated only at much higher cell density. The consequence of this asymmetry is that exogenous sources of AI-2, but not CAI-1, contribute to satisfying the coincidence detector to repress biofilm formation and promote dispersal. We propose that V. cholerae uses CAI-1 to verify that some of its kin are present before committing to the high-cell-density QS mode, but it is, in fact, the broadly made autoinducer AI-2 that sets the pace of the V. cholerae QS program. This first report of unique roles for the different V. cholerae autoinducers suggests that detection of kin fosters a distinct outcome from detection of nonkin.

Dataset Information

Vibrio cholerae Combines Individual and Collective Sensing to Trigger Biofilm Dispersal.

Publications

Vibrio cholerae Combines Individual and Collective Sensing to Trigger Biofilm Dispersal.

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