Review
Lifestyle evolution in symbiotic bacteria: insights from genomics

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Abstract

Bacteria that live only in eukaryotic cells and tissues, including chronic pathogens and mutualistic bacteriocyte associates, often possess a distinctive set of genomic traits, including reduced genome size, biased nucleotide base composition and fast polypeptide evolution. These phylogenetically diverse bacteria have lost certain functional categories of genes, including DNA repair genes, which affect mutational patterns. However, pathogens and mutualistic symbionts retain loci that underlie their unique interaction types, such as genes enabling nutrient provisioning by mutualistic bacteria-inhabiting animals. Recent genomic studies suggest that many of these bacteria are irreversibly specialized, precluding shifts between pathogenesis and mutualism.

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)

  • K. Saikkonen

    Fungal endophytesa continuum of interactions with host plants

    Annu. Rev. Ecol. Syst.

    (1998)
  • D. Corsaro

    Intracellular life

    Crit. Rev. Microbiol.

    (1999)
  • C.R. Woese

    Bacterial evolution

    Microbiol. Rev.

    (1987)
  • P. Hugenholtz

    Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity

    J. Bacteriol.

    (1998)
  • B.L. Maidak

    A new version of the RDP (ribosomal database project)

    Nucleic Acids Res.

    (1999)
  • C. Bandi

    The establishment of intracellular symbiosis in an ancestor of cockroaches and termites

    Proc. R. Soc. London Ser. B.

    (1995)
  • P. Baumann

    The evolution and genetics of aphid endosymbionts

    BioScience

    (1997)
  • N.A. Moran et al.

    The evolution of bacteriocyte-associated endosymbionts in insects

    BioScience

    (1998)
  • A.S. Peek

    Accelerated evolutionary rate in sulfur-oxidizing endosymbiotic bacteria associated with the mode of symbiont transmission

    Mol. Biol. Evol.

    (1998)
  • A.W. Spaulding et al.

    Phylogenetic characterization and molecular evolution of bacterial endosymbionts in psyllids (HemipteraSternorrhyncha)

    Mol. Biol. Evol.

    (1998)
  • D.R. Stothard

    Ancestral divergence of Rickettsia bellii from the spotted fever and typhus groups of Rickettsia and antiquity of the genus Rickettsia

    Int. J. Syst. Bacteriol.

    (1994)
  • B.F. Lang

    Mitochondrial genome evolution and the origin of eukaryotes

    Annu. Rev. Genet.

    (1999)
  • G.D.D. Hurst

    Adonia variegata (ColeopteraCoccinellidae) bears maternally inherited Flavobacteria that kill males only

    Parasitology

    (1999)
  • S.L. O’Neill

    Influential Passengers: Inherited Microorganisms and Arthropod Reproduction

    (1998)
  • H. Charles et al.

    Physical and genetic map of the genome of Buchnera, the primary endosymbiont of the pea aphid, Acyrthosiphon pisum

    J. Mol. Evol.

    (1999)
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