Trends in Genetics
Volume 29, Issue 3, March 2013, Pages 170-175
Journal home page for Trends in Genetics

Review
Horizontal gene transfer and the evolution of bacterial and archaeal population structure

https://doi.org/10.1016/j.tig.2012.12.006Get rights and content

Many bacterial and archaeal lineages have a history of extensive and ongoing horizontal gene transfer and loss, as evidenced by the large differences in genome content even among otherwise closely related isolates. How ecologically cohesive populations might evolve and be maintained under such conditions of rapid gene turnover has remained controversial. Here we synthesize recent literature demonstrating the importance of habitat and niche in structuring horizontal gene transfer. This leads to a model of ecological speciation via gradual genetic isolation triggered by differential habitat-association of nascent populations. Further, we hypothesize that subpopulations can evolve through local gene-exchange networks by tapping into a gene pool that is adaptive towards local, continuously changing organismic interactions and is, to a large degree, responsible for the observed rapid gene turnover. Overall, these insights help to explain how bacteria and archaea form populations that display both ecological cohesion and high genomic diversity.

Section snippets

Genotypic clustering

Plants and animals are organized into phenotypic and genotypic clusters, and this forms the vernacular notion of a species. For bacteria and archaea the identification of natural clusters was difficult before sequencing became widely available because phenotypic traits used for traditional taxonomy were arbitrarily defined. Although traditional classification allowed reliable identification [7], it is clear that many taxonomic species do not necessarily represent natural units. Hence it was an

Formation of genotypic clusters

Recent population genomic data allow a synthesis of past theories and observations that were seemingly at odds in explaining cluster formation. In presenting this new evidence, we first pose the important question of whether genotypic clusters can originate among sympatric microbes in the absence of selection. The focus on sympatric differentiation is because geographic isolation, although thought to be an important factor in animals and plants, appears to be the exception in microbes having

A habitat-specific gene pool?

The above model shows how genotypic clusters in the core genome might arise, but has yet to consider fully the intricacies of the flexible genome – which has very high turnover, can contribute a large portion of the total genes, and makes up the bulk of the vast pan-genome. In fact, one of the puzzles of microbial biology is that genomes can be highly optimized energetically and functionally while tolerating the disruptive effect of horizontally acquired genes that are both phylogenetically and

Concluding remarks

Although we are only beginning to understand the intricacies of gene flow in the wild, it is becoming clear that gene-transfer networks need to be analyzed in the context of ecology. The recent results reviewed here add an evolutionary dimension to this ecological structure by showing how clusters may arise as a consequence of ecological specialization. The gradual mechanism by which this happens (Figure 1) is unexpected because theoretical considerations have suggested genome-wide selective

Acknowledgments

Funding was provided by grants from the Moore Foundation (M.F.P.), the National Science Foundation (DEB 0821391 to E.J.A. and M.F.P.), the National Institutes of Health (NIH)/National Institute of General Medical Sciences (NIGMS) (GM088558-01 to W.P.H.), and the MIDAS Center for Communicable Disease Dynamics at the Harvard School of Public Health (W.P.H.). We also thank James McInerney for helpful discussions.

References (51)

  • O. Popa

    Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes

    Genome Res.

    (2011)
  • A. Mira

    The bacterial pan-genome:a new paradigm in microbiology

    Int. Microbiol.

    (2010)
  • W.F. Doolittle et al.

    On the origin of prokaryotic species

    Genome Res.

    (2009)
  • W.F. Doolittle et al.

    Genomics and the bacterial species problem

    Genome Biol.

    (2006)
  • W.P. Hanage

    Sequences, sequence clusters and bacterial species

    Philos. Trans. R. Soc. Lond. B: Biol. Sci.

    (2006)
  • M.F. Polz

    Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes

    Philos. Trans. R. Soc. Lond. B: Biol. Sci.

    (2006)
  • N.J. Croucher

    Rapid pneumococcal evolution in response to clinical interventions

    Science

    (2011)
  • H. Cadillo-Quiroz

    Patterns of gene flow define species of thermophilic archaea

    PLoS Biol.

    (2012)
  • V.J. Denef

    AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature

    ISME J.

    (2010)
  • A. Caro-Quintero et al.

    Bacterial species may exist, metagenomics reveal

    Environ. Microbiol.

    (2012)
  • M.F. Polz et al.

    Overview: quantitative and theoretical microbial population biology

  • R.J. Whitaker

    Allopatric origins of microbial species

    Philos. Trans. R. Soc. Lond. B: Biol. Sci.

    (2006)
  • C. Fraser

    Recombination and the nature of bacterial speciation

    Science

    (2007)
  • F.M. Cohan

    The effects of rare but promiscuous genetic exchange on evolutionary divergence in prokaryotes

    Am. Nat.

    (1994)
  • F.M. Cohan

    What are bacterial species

    Annu. Rev. Microbiol.

    (2002)
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