Trends in Ecology & Evolution
ReviewLifestyle evolution in symbiotic bacteria: insights from genomics
Section snippets
Should we expect labile interactions?
Numerous investigators have proposed that mutualism and parasitism (defined here in terms of effects on host fitness) are dynamic alternatives to a partner in a biological interaction1, 2, 3, 4, 5, 6, 7. Conditions favoring overlap in host and symbiont reproductive interests, such as vertical transmission (Box 1) and long-term persistence in an individual host, push towards mutualism. Conditions favoring selfishness, such as a high rate of horizontal infection and competition within hosts, push
Have bacterial symbionts switched between mutualism and parasitism?
Frequent transitions between parasitism and mutualism would produce a mosaic of interaction types within clades of animal-associated bacteria, resulting in closely related parasitic and mutualistic species sometimes inhabiting the same or related hosts. Molecular phylogenetic studies allow us to test this prediction by placing noncultivable symbiotic bacteria in a phylogenetic context; this development began with the work of Woese10 and continues with the exploration of prokaryotic diversity in
Does genome content prevent switches between mutualism and parasitism?
The monophyly and antiquity of mutualistic and parasitic bacterial clades indicate that symbiotic interactions between bacteria and animals might be more constrained than evolutionary models predict. Such models are based on the implicit presumption that partners retain the genetic potential for a full spectrum of interaction types. Is this assumption true for intimate bacterial associates of animals? Evidence from full genome sequences, summarized in the next section, suggests a basis for
From population genetics: explanations?
From the previous discussion, it appears that mutualistic and parasitic bacteria share a common syndrome of genomic reduction and accelerated sequence evolution. Why? For symbionts that form chronic infections, reduced effective population size and reduced recombination have been hypothesized to increase levels of genetic drift and to decrease the effectiveness of selection; this effect has been proposed for pathogens23, 40 and mutualistic symbionts26, 27, 28, 29, including organelles41. As a
Lability of host interactions among opportunistic animal pathogens and plant symbionts
Our focus has been on bacterial associates of eukaryotes that fit the resident genome syndrome proposed by Andersson and Kurland23. These are chronic pathogens or mutualists that spend their life cycles closely associated with host cells. Many bacteria show more labile associations with eukaryotes; in these, shifts between mutualism and parasitism appear to be achieved relatively frequently through the transfer of genes affecting interactions with hosts. For example, the acquisition of
Prospects
In summary, phylogenetic and genomic data support the hypothesis that many clades of intimate bacterial symbionts are strictly mutualistic or parasitic. Transitions between these interaction types might be restricted owing to irreversible loss of genes and associated functional capabilities. Further testing of this proposal will be possible as phylogenetic relationships, genome complements and phenotypic effects of additional symbiont lineages are characterized. For example, a large proportion
Uncited references
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Acknowledgements
We thank H. Ishikawa for unpublished information on the gene content of Buchnera. Work underlying this article was supported by NSF DEB-9978518 (N.A.M.) and an NIH training grant to the Center for Insect Science (J.J.W.). H. Ochman, members of the Moran lab and anonymous reviewers provided helpful comments.
References (50)
The evolution of mutualismsexploring the paths between conflict and cooperation
Trends Ecol. Evol.
(1999)Vertical transmission and evolution of mutualism from parasitism
Theor. Popul. Biol.
(1993)Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia
Int. J. Parasitol.
(1999)- et al.
Reductive evolution of resident genomes
Trends Microbiol.
(1998) - et al.
How Salmonella became a pathogen
Trends Microbiol.
(1997) Host benefit and the evolution of specialization in symbiosis
Heredity
(1998)Models of symbiosis
Am. Nat.
(1997)The population-dynamics of vertically and horizontally transmitted parasites
Proc. R. Soc. London Ser. B.
(1995)Gene flow and geographically structured coevolution
Proc. R. Soc. London Ser. B.
(1999)- et al.
Forty million years of mutualismevidence for Eocene origin of the yucca–yucca moth association
Proc. Natl. Acad. Sci. U. S. A.
(1999)