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Bacteria, once thought capable of only simple processes and single-celled life, are now appreciated for their ability to act collectively in multi-cellular groups. Coordinated behaviours include bioluminescence, virulence factor production, secondary metabolite production, competence for DNA uptake and biofilm formation. To orchestrate collective behaviours, bacteria use the cell-to-cell communication process called quorum sensing. Quorum sensing is mediated by the production, release, accumulation and group-wide detection of extracellular signalling molecules called autoinducers. Bacteria typically integrate information encoded in several quorum-sensing autoinducers into the control of gene expression, which enables intra-species, intragenera and inter-species communication as well as communication with bacteria in the microbiota. Our current understanding of quorum-sensing mechanisms stems primarily from studying traditional wellmixed pure laboratory cultures. These studies have provided foundational knowledge of the molecular mechanisms underlying quorum sensing in different bacteria. However, bacteria often exist in mixtures of species as well as under non-ideal conditions in which fluctuations occur.
Fig. 1 | Quorum-sensing circuits.
(Source: Nature Reviews Microbiology, 2019.)
Bacteria attach to surfaces and, together, build biofilm communities. We now understand that biofilms are a predominant form of bacterial life on Earth and that these sessile communities are relevant in the environment, medicine and industry. Unlike well-mixed bacterial cultures in liquid, biofilms are heterogeneous and can rearrange over time, raising questions about nutrient acquisition and diffusion.
Effects of fluid flow and surface topography on quorum-sensing signalling. Bacteria form biofilms on diverse surfaces, including soil, river beds, sewage, deep-sea vents and plant and animal tissues. Natural environments differ from those traditionally used in the laboratory for investigating biofilms by two key features: the presence of irregular surfaces and the presence of fluid flow. Bacteria exhibit distinct biofilm formation behaviours with respect to their quorum-sensing states. Flow, while ubiquitous in living systems, need not be constant. Thus, intermittent flow can lead to non-uniform quorum-sensing gene expression over time. In addition to fluid flow, surface topography also influences quorum-sensing dynamics, and as mentioned, often flow and topographical constraints are connected.
Heterogeneity in quorum sensing. In contrast to the traditional idea that quorum sensing promotes the synchronous expression of target genes across a bacterial population, recent studies suggest that quorum sensing-dependent processes can be stochastic: a subpopulation of cells can exhibit the quorum-sensing-on mode, whereas the remaining population is in the quorum-sensing-off mode. In most cases, the molecular mechanisms underlying heterogeneity are not yet defined. Furthermore, genetic heterogeneity can occur when quorum-sensing mutants arise in bacterial populations. An emerging theme in this realm is that quorum sensing heterogeneity is a feature associated with the LCD state of bacterial populations. Maintaining phenotypic heterogeneity in HCD quorum-sensing populations could allow the bacteria to undertake bet-hedging strategies in which, simultaneously, some cells in the population perform individual behaviors whereas others engage in collective activities.
The public goods dilemma, cooperation and cheating. Bacteria frequently secrete extracellular biomolecules to capture nutrients from the environment, hydrolyse solid food sources and construct biofilm communities. Some secreted substances can be used by nonproducing cells and are thus considered to be public goods. Several processes, including spatial structure and social policing of the community, are thought to promote cooperation and prevent cheating in bacterial systems that depend on public goods. Curiously, under some conditions, spatial structure can also allow wild-type bacteria and cheaters to coexist. Autoinducers can also function as public goods and, thus, are prone to exploitation by nonproducing cheaters. Another strategy that prevents cheating in situations in which public goods are at stake is social policing. In summary, quorum-sensing-driven co-regulation of two metabolic enzymes, one that serves as a public good and one that serves as a private good, can provide an incentive that reduces social cheating and prevents the collapse of the wild-type population.
Inside hosts, bacteria often exist in mixed-species communities and, therefore, quorum sensing by one species can influence and be influenced by quorum sensing or other activities carried out by neighbouring species. Furthermore, host processes such as the immune response can also influence bacterial quorum sensing and vice versa.
Quorum sensing and the host-associated microbiota. Eukaryotes harbour diverse microbial ecosystems that make up the microbiota. Increasing evidence suggests that inter-species and inter-kingdom chemical communication shape the species composition of the gut microbiota. Inter-kingdom communication between bacteria and hosts could also influence colonization.
Host factors influence bacterial quorum sensing. Microbiota communities that reside on epithelial surfaces are influenced by host factors including innate immune components, mucus composition and diet. Notably, eukaryotes can produce enzymes that quench bacterial quorum-sensing-mediated communication. Host factors can also affect quorum-sensing signalling and thereby modulate the outcome of pathogen invasion. Likewise, there is evidence from transcriptomic studies that during human infection by P. aeruginosa, quorum sensing is suppressed relative to that in laboratory setups in vitro. Quorum-sensing-mediated control of bacterial behavior has a central role in bacterial lifestyle transitions.
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