Elsevier

Current Opinion in Microbiology

Volume 2, Issue 6, 1 December 1999, Pages 582-587
Current Opinion in Microbiology

Review
How bacteria talk to each other: regulation of gene expression by quorum sensing

https://doi.org/10.1016/S1369-5274(99)00025-9Get rights and content

Abstract

Quorum sensing, or the control of gene expression in response to cell density, is used by both Gram-negative and Gram-positive bacteria to regulate a variety of physiological functions. In all cases, quorum sensing involves the production and detection of extracellular signalling molecules called autoinducers. While universal signalling themes exist, variations in the design of the extracellular signals, the signal detection apparatuses, and the biochemical mechanisms of signal relay have allowed quorum sensing systems to be exquisitely adapted for their varied uses. Recent studies show that quorum sensing modulates both intra- and inter-species cell–cell communication, and it plays a major role in enabling bacteria to architect complex community structures.

Introduction

Research in bacterial quorum sensing began with studies of the density-dependent expression of bioluminescence in the marine symbiotic bacterium Vibrio fischeri and its free-living relative Vibrio harveyi 1, 2. Both species produce and respond to secreted acylated-homoserine lactone (HSL) signalling molecules called autoinducers that accumulate in the external environment as the cells grow 3, 4. When the concentration of autoinducer exceeds a threshold level, a signal transduction cascade is initiated that leads to the production of luciferase. The crucial findings of Engebrecht and Silverman 5, 6, 7 laid the foundation for all subsequent studies of quorum sensing in Gram-negative bacteria. They identified, cloned, and analysed the genes encoding the luciferase enzyme complex and the genes responsible for its density-dependent regulation from V. fischeri. They showed that light production in V. fischeri is controlled by two regulatory proteins named LuxI and LuxR. LuxI is the autoinducer synthase that is responsible for the synthesis of the acyl-HSL autoinducer. LuxR is a transcriptional activator protein that, when bound to autoinducer, promotes transcription of the luciferase structural operon luxCDABE 5, 6, 7. These observations first explained how gene expression could be coupled to cell-population density.

This review focuses on recent advances in how bacteria regulate gene expression in response to cell density. Specifically, this review highlights major differences and similarities in the mechanisms employed for quorum sensing in Gram-negative and Gram-positive bacteria. Recent findings that demonstrate how sophisticated signalling networks are employed in these cell–cell communication systems are discussed.

Section snippets

Gram-negative bacterial communication: the LuxI/LuxR language

The simple signal-response mechanism described by Engebrecht and Silverman has now been shown to be employed by over 30 species of Gram-negative bacteria for the control of different cell-density-dependent functions 8, 9. These systems all have in common the use of an HSL autoinducer whose synthesis is dependent on a luxI homologue, as well as a luxR homologue encoding a transcriptional activator protein that is responsible for detection of the cognate HSL and induction of expression of the

Gram-positive bacteria have their own language

There exist a number of processes in Gram-positive bacteria that are responsive to cell population density. Among these are competence for DNA uptake in Bacillus subtilis and Streptococcus pneumoniae, virulence in Staphylococcus aureus, conjugation in Enterococcus faecalis and microcin production in Lactobacillus sake and Carnobacterium piscicola. Gram-positive bacteria do not employ HSLs as signals, nor do they use a LuxI/LuxR signalling circuit. Instead, Gram-positive bacteria secrete

Hybrid languages: the quorum sensing systems of V. harveyi

The free-living marine luminous bacterium V. harveyi possesses two autoinducer-response systems that function in parallel to control the density-dependent expression of the luciferase structural operon luxCDABE. This complex quorum sensing circuit has features found in both Gram-negative and Gram-positive bacteria. Like other Gram-negative quorum sensing bacteria, V. harveyi produces and responds to an acylated-HSL autoinducer. The second V. harveyi autoinducer is of unknown structure, but

Bacterial Esperanto: the LuxS family of autoinducers

Highly conserved luxS homologues have now been identified in both Gram-negative and Gram-positive bacterial species including Escherichia coli, Salmonella typhimurium, Salmonella typhi, Salmonella paratyphi, Haemophilus influenzae, Helicobacter pylori, B. subtilis, Borrelia burgdorferi, Neisseria meningitidis, Neisseria gonorrhoeae, Yersinia pestis, Campylobacter jejuni, Vibrio cholerae, Deinococcus radiodurans, Mycobacterium tuberculosis, E. faecalis, S. pneumoniae, Streptococcus pyogenes,

Multilingual bacteria: cell–cell communication in nature

As noted below, there are several fascinating systems currently under study in which the use of intra- and inter-species quorum sensing would be predicted to greatly enhance a particular bacterium’s chances of survival, or would allow bacteria to build communities in which specialisation/division of labour would grant the entire community some of the properties and benefits that would otherwise be exclusive to multicellular organisms.

Quorum sensing regulates virulence in many human and plant

Conclusions

Considerable progress has been made this past year in our understanding of the variety of functions controlled by quorum sensing and the different mechanisms that bacteria use for counting cell number and modulating gene expression in response to changes in cell-population density. It is now clear that quorum sensing regulates bacterial communication in test tubes and in nature. It is also clear that intra- and inter-species cell–cell communication occurs and is regulated by quorum sensing

Acknowledgements

This work was supported by the National Science Foundation Grant Number MCB-9506033 and The Office of Naval Research Grant number N00014-99-0767.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

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