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Communication in bacteria: an ecological and evolutionary perspective

Nature Reviews Microbiology volume 4, pages 249–258 (2006)Cite this article

Key Points

  • Understanding why and how bacteria react to the chemical substances that are produced by other bacteria requires an understanding of the nature of the chemical interaction, and the determination of the effect on the fitness of the emitter and receiver.

  • The nature of chemical interactions between bacteria is not necessarily in the form of cooperative signals, but also includes other chemical interactions, such as cues and chemical manipulation.

  • The specificity and reliability of communication depends on the cost of signal production. This cost can be approximated by the biosynthetic cost of signalling, and there is a correlation between the cost of signal production and the specificity of the signalling molecules for the three most common signalling pathways.

  • High relatedness, as occurs, for example, when all cells develop from a single founding cell, is a key factor that promotes cooperation and true communication. Inversely, true communication and cooperation are unlikely to be common between species.

  • A review of the data shows that the evolutionary framework, developed above, allows us to gain a better understanding of quorum sensing and the nature of communication between bacteria, as well as between bacteria and their host.

Abstract

Individual bacteria can alter their behaviour through chemical interactions between organisms in microbial communities ? this is generally referred to as quorum sensing. Frequently, these interactions are interpreted in terms of communication to mediate coordinated, multicellular behaviour. We show that the nature of interactions through quorum-sensing chemicals does not simply involve cooperative signals, but entails other interactions such as cues and chemical manipulations. These signals might have a role in conflicts within and between species. The nature of the chemical interaction is important to take into account when studying why and how bacteria react to the chemical substances that are produced by other bacteria.

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Figure 1: Generic scheme for quorum sensing.
Figure 2: The pathways for production of the three common quorum-sensing signals in bacteria.
Figure 3: Clonal relationship and intraspecies signalling.
Figure 4: Chemical signalling within microbial communities of oral bacteria.

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Acknowledgements

We thank B. Bassler, C. Davidson, P. Greenberg, G. Velicer, K. Visick, P. Williams and four reviewers for their useful comments on the manuscript. The authors were supported by grants from the Swiss National Science Foundation (L.K.) and the Canadian Institutes of Health Research (M.G.S.).

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Authors and Affiliations

  1. Department of Ecology and Evolution, University of Lausanne, Lausanne, 1015, Switzerland

    Laurent Keller

  2. Department of Microbiology and Infectious Diseases, Department of Biochemistry and Molecular Biology, University of Calgary, 3330 Hospital Drive NW, Calgary, T2N 4N1, Alberta, Canada

    Michael G. Surette

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DATABASES

Entrez Genome Project

Agrobacterium tumefaciens

Chromobacterium violaceum

Myxococcus xanthus

Pseudomonas aeruginosa

Pseudomonas putida

Saccharomyces cerevisiae

Salmonella enterica serovar Typhimurium

Staphylococcus aureus

Streptococcus gordonii

Vibrio fischeri

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Micheal G. Surette's homepage

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Glossary

Secondary metabolite

Chemical produced by the cell that is not essential for maintenance of cellular function or for normal growth of the organism.

Quorum sensing

A system by which bacteria communicate and obtain information on bacterial density in their environment.

Autoinducer

A system by which bacteria communicate. Signalling molecules are chemicals, similar to pheromones that are produced by an individual bacterium, which can affect the behaviour of surrounding bacteria.

Signal

Any act, structure or chemical emission that alters the behaviour and gene expression of other organisms which evolved because of that effect, and that is effective because the receiver's response has also evolved.

N-acyl homoserine lactone

A group of intercellular signalling molecules, produced by some Gram-negative bacteria, made up of a homoserinelactone ring with an N-linked acyl side chain.

LuxS/autoinducer-2

(AI-2). Refers to a conserved gene (luxS) found in both Gram-negative and Gram-positive bacteria that mediates production of a common signalling molecule autoinducer-2.

Pre-protein

A protein initially synthesized as an inactive form that undergoes proteolytic cleavage to release the active protein or peptide.

Chemical manipulation

Chemical emission that alters the behaviour and gene expression of other organisms. However, contrary to a signal, the effect induced by chemical manipulation has a negative effect on the fitness of the receiver.

Cue

An act, structure or chemical emission that alters the behaviour and gene expression of other organisms. However, contrary to a signal, it did not evolve specifically for that effect.

Fruiting body

A specialized macroscopic, spore-producing structure that is formed by some fungi (for example, mushrooms), slime moulds and mycobacteria.

Cheater

An individual obtaining benefits from a collectively produced public good that are disproportionally large relative to its own contribution to that good.

Conjugative plasmid

A plasmid that can move from one cell to another during the process of conjugation.

Symbiont

An organism living in a close, long-lasting and more or less beneficial association with another organism.

Syntrophic association

A process whereby two or more microorganisms cooperate to degrade a substrate or substrates that neither can degrade alone.

Niche partitioning

The division of a limiting resource(s) among the species that share it.

Flushing

The removal of chemicals and/or individuals from an area by a current or flow through the area.

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Keller, L., Surette, M. Communication in bacteria: an ecological and evolutionary perspective. Nat Rev Microbiol 4, 249–258 (2006). https://doi.org/10.1038/nrmicro1383

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