Symbiotic conversations are revealed under genetic interrogation

Key Points

  • Microbial symbiosis is a central factor in the evolution of all animal species and in the survival of all individuals. Advances in molecular genetics are allowing the development of invertebrate–bacteria associations as model systems for understanding how the host and microorganism communicate.

  • Five natural systems have been particularly well described, including three that are binary (the host and one bacterial species) and two that consist of simple bacterial consortia of fewer than a dozen species.

  • The development of these experimental symbiosis models has allowed us to ask distinct sets of questions about host–microorganism communication and has provided a breadth of opportunities that would not be available from any one system.

  • In the past 20 years, advances in our understanding of host–microorganism communication have centred on several common themes: surface structures and specificity; bacterial behaviour and gene regulation; adaptation to host defences; induction of host development; and nutritional and metabolic accommodation. Although parallels can be drawn between the systems, there are also intriguing differences that reflect the special biology of each host–microorganism association.

  • A number of newly recognized symbioses between bacteria and invertebrate hosts are emerging as model systems in which molecular genetic approaches are only now being applied.

Abstract

The recent development and application of molecular genetics to the symbionts of invertebrate animal species have advanced our knowledge of the biochemical communication that occurs between the host and its bacterial symbionts. In particular, the ability to manipulate these associations experimentally by introducing genetic variants of the symbionts into naive hosts has allowed the discovery of novel colonization mechanisms and factors. In addition, the role of the symbionts in inducing normal host development has been revealed, and its molecular basis described. In this Review, I discuss many of these developments, focusing on what has been discovered in five well-understood model systems.

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Figure 1: Microbial symbioses occur throughout the phylogeny of animals.
Figure 2: Classes of symbiosis models.
Figure 3: Simplified life cycles of five symbioses.
Figure 4: Categories of colonization mutants.

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Acknowledgements

The author thanks M. McFall-Ngai for helpful discussions and ideas, and H. Goodrich-Blair, J. Graf and M. Mandel for reading parts of the manuscript. Support was provided by grants from the National Institutes of Health (grant number RR-12294) and the National Science Foundation (grant number IOB-0517007).

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DATABASES

Entrez Genome Project

Drosophila melanogaster

Enterococcus faecalis

Escherichia coli

Sodalis glossinidius

Vibrio fischeri

Yersinia pestis

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Glossary

Bioluminescence

The process by which some bacteria and other organisms produce light as the result of a chemical reaction. During symbiosis, this light can be used in behaviours such as counterillumination, in which the bioluminescence is used to eliminate the shadow of the host's silhouette.

Gnotobiotic

An animal that is born under aseptic conditions and is exposed only to experimentally introduced microorganisms. Gnotobiotic animals are used to investigate the symbiotic relationship between an animal and one or more of the consortia of interacting microbial species that normally inhabit its body.

Horizontal transfer

The process by which an animal or plant obtains its natural microbial constituents from the environment at each generation. By contrast, vertical transfer occurs when a young organism receives its microbiota from its parent, usually in or on the egg.

Expressed sequence tag

(EST). One of a series of short nucleotide sequences which represent a pool of mRNAs that are expressed under a certain environmental or developmental condition. Libraries of ESTs can be used to identify gene transcripts in global expression studies.

Two-component regulation system

A stimulus-response coupling mechanism that allows an organism to sense and respond to various changes in environmental conditions.

Lipopolysaccharide

A major component of the outer membrane of Gram-negative bacteria. The immune systems of animals generally sense and react to the presence of lipopolysaccharide.

Quorum sensing

A system by which bacteria respond to increased population density by coordinately controlling expression of a specific set of genes. By sensing the concentration of one of several continuously secreted signal molecules, including acyl homoserine lactones, peptides and autoinducer 2, the population can recognize when it reaches a 'quorum'.

Auxotroph

An organism, or mutant derivative, which is unable to synthesize a particular compound (for example, an amino acid) that is required as a building block for its growth.

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Ruby, E. Symbiotic conversations are revealed under genetic interrogation. Nat Rev Microbiol 6, 752–762 (2008). https://doi.org/10.1038/nrmicro1958

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