Bacterial quorum sensing in complex and dynamically changing environments

Abstract

Quorum sensing is a process of bacterial cell-to-cell chemical communication that relies on the production, detection and response to extracellular signalling molecules called autoinducers. Quorum sensing allows groups of bacteria to synchronously alter behaviour in response to changes in the population density and species composition of the vicinal community. Quorum-sensing-mediated communication is now understood to be the norm in the bacterial world. Elegant research has defined quorum-sensing components and their interactions, for the most part, under ideal and highly controlled conditions. Indeed, these seminal studies laid the foundations for the field. In this Review, we highlight new findings concerning how bacteria deploy quorum sensing in realistic scenarios that mimic nature. We focus on how quorums are detected and how quorum sensing controls group behaviours in complex and dynamically changing environments such as multi-species bacterial communities, in the presence of flow, in 3D non-uniform biofilms and in hosts during infection.

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Fig. 1: Quorum-sensing circuits.
Fig. 2: Fluid flow and surface topography influence quorum-sensing dynamics.
Fig. 3: Heterogeneity in quorum sensing.
Fig. 4: Quorum sensing and the public goods dilemma.
Fig. 5: Quorum sensing and the host microbiota.
Fig. 6: Host factors influence quorum sensing.

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Acknowledgements

This work was supported by the Howard Hughes Medical Institute, US National Institutes of Health (NIH) grant 5R37GM065859 and National Science Foundation grant MCB-1713731 (to B.L.B.), as well as by a Life Science Research Foundation Postdoctoral Fellowship through the Gordon and Betty Moore Foundation through grant GBMF2550.06 and NIH grant 1K99GM129424-01 to S.M.

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Correspondence to Bonnie L. Bassler.

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Supplementary information

Thick biofilms allow quorum sensing to occur under flow.

Supplementary Movie 1 Shown are a series of merged fluorescence images of S. aureus biofilms under 13 h of flow (left) and following 13 h of flow and 3 h of no flow (right) following inoculation. Slices in the image stack are 3 μm apart in the z-direction. Bacteria in the quorum-sensing-off state are false-colored red while quorum-sensing-on cells are false-colored yellow. Movie is reproduced from Kim, M. K., Ingremeau, F., Zhao, A., Bassler, B. L. & Stone, H. A. Local and global consequences of flow on bacterial quorum sensing. Nat. Microbiol. 1, 15005 (2016).

Quorum sensing is activated inside crevices.

Supplementary Movie 2 Shown is a time series of merged fluorescence images of S. aureus in a complex topography, taken at 10-minute intervals. Bacteria in the quorum-sensing-off state are false-colored red while quorum-sensing-on cells are false-colored yellow. Movie is reproduced from Kim, M. K., Ingremeau, F., Zhao, A., Bassler, B. L. & Stone, H. A. Local and global consequences of flow on bacterial quorum sensing. Nat. Microbiol. 1, 15005 (2016).

Glossary

Phenotypic heterogeneity

Nongenetic variations in traits between individual cells in an isogenic population.

Bet hedging

A strategy that enables diversification of phenotypes within a population with the consequence of reducing the overall risk of death of all the cells in the population. Thus, bet hedging increases fitness under temporally varying conditions.

Social policing

A strategy in which quorum-sensing bacteria link production of costly private goods to production of public goods to punish nonproducers and thereby prevent emergence of social cheaters.

Dysbiosis

A microbial imbalance on or inside a host in which the normal microbiota is disrupted, for example, after treatment with antibiotics.

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Mukherjee, S., Bassler, B.L. Bacterial quorum sensing in complex and dynamically changing environments. Nat Rev Microbiol 17, 371–382 (2019). https://doi.org/10.1038/s41579-019-0186-5

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