The Interplay of Homologous Recombination and Horizontal Gene Transfer in Bacterial Speciation

  • Jeffrey G. Lawrence
  • Adam C. Retchless
Part of the Methods in Molecular Biology book series (MIMB, volume 532)


Bacteria experience recombination in two ways. In the context of the Biological Species concept, allelic exchange purges genic variability within bacterial populations as gene exchange mediates selective sweeps. In contrast, horizontal gene transfer (HGT) increases the size of the population’s pan-genome by providing an influx of novel genetic material. Here we discuss the interplay of these two processes, with an emphasis on how they allow for the maintenance of genotypically cohesive bacterial populations, yet allow for the separation of these populations upon bacterial speciation. In populations that maintain genotypic similarity by frequent allelic exchange, horizontally transferred genes may initiate ecological barriers to genetic exchange. The resulting recombination interference allows for the accumulation of neutral mutations and, consequently, the imposition of a pre-mating barrier to gene transfer.


Recombination speciation periodic selection recombination interference horizontal gene transfer cohesion species concepts 


  1. 1.
    Aristotle (1910) Historia Animalium (translated by D’Arcy Wentworth Thompson), Clarendon Press, Oxford.Google Scholar
  2. 2.
    Linnaeus, C. (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis, Holmiae.Google Scholar
  3. 3.
    Quinn, P. C. (2002) Young infants’ categorization of humans versus nonhuman animals: roles for knowledge access and perceptual process, in Building Object Categories in Developmental Time (Lisa Gershkoff-Stowe, D. H. R., ed.) Lawrence Erlbaum Associates, Mahwah, NJ.Google Scholar
  4. 4.
    Senate and House of Representatives of the United States of America (1973) Endangered Species Act of 1973. In. (Agency, E. P., ed.) Government of the United States of America Place.Google Scholar
  5. 5.
    Darwin, C. (1859) On the Origin of Species by Means of Natural Selection or the Preservation of Favoured Races in the Struggle for Life, John Murray, London.Google Scholar
  6. 6.
    Gevers, D., Cohan, F. M., Lawrence, J. G., Spratt, B. G., Coenye, T., Feil, E. J., Stackebrandt, E., Van De Peer, Y., Vandamme, P., Thompson, F. L., Swings, J. (2005) Re-evaluating prokaryotic species. Nat Rev Microbiol 3, 733–9.CrossRefPubMedGoogle Scholar
  7. 7.
    Mayr, E. (1942) Systematics and the Origin of Species, Columbia University Press, New York.Google Scholar
  8. 8.
    Mayr, E. (1963) Animal Species and Evolution, Harvard University Press, Cambridge.Google Scholar
  9. 9.
    Paterson, H. E. H. (1985) The recognition concept of species, in Species and Speciation (Vrba, E. S., ed.) Transvaal Museum, Pretoria, 21–9.Google Scholar
  10. 10.
    Van Valen, L. (1976) Ecological species, multispecies, and oaks. Taxon 25, 223–39.CrossRefGoogle Scholar
  11. 11.
    Wiley, E. O. (1978) The evolutionary species concept reconsidered. Syst Zool 27, 17–26.CrossRefGoogle Scholar
  12. 12.
    Templeton, A. R. (1989) The meaning of species and speciation: a genetic perspective, in Speciation and Its Consequences (Otte, D., Endler J. A., ed.) Sinauer Associates, Sunderland, MA, 3–27.Google Scholar
  13. 13.
    Levin, B. R. (1981) Periodic selection, infectious gene exchange and the genetic structure of E. coli populations. Genetics 99, 1–23.PubMedGoogle Scholar
  14. 14.
    Atwood, K. C., Schneider, L. K., Ryan, F. J. (1951) Periodic selection in Escherichia coli. Proc Natl Acad Sci USA 37, 146–55.CrossRefPubMedGoogle Scholar
  15. 15.
    Cohan, F. M. (2001) Bacterial species and speciation. Syst Biol 50, 513–24.CrossRefPubMedGoogle Scholar
  16. 16.
    Cohan, F. M., Perry, E. B. (2007) A systematics for discovering the fundamental units of bacterial diversity. Curr Biol 17, R373–86.CrossRefPubMedGoogle Scholar
  17. 17.
    Ochman, H., Lawrence, J. G., Groisman, E. (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299–304.CrossRefPubMedGoogle Scholar
  18. 18.
    O’neill, M., Chen, A., Murray, N. E. (1997) The restriction-modification genes of Escherichia coli K-12 may not be selfish: they do not resist loss and are readily replaced by alleles conferring different specificities. Proc Natl Acad Sci USA 94, 14596–601.CrossRefPubMedGoogle Scholar
  19. 19.
    Barcus, V. A., Titheradge, A. J., Murray, N. E. (1995) The diversity of alleles at the hsd locus in natural populations of Escherichia coli. Genetics 140, 1187–97.Google Scholar
  20. 20.
    Murray, N. E. (2000) Type I restriction systems: sophisticated molecular machines (a legacy of Bertani and Weigle). Microbiol Mol Biol Rev 64, 412–34.CrossRefPubMedGoogle Scholar
  21. 21.
    Milkman, R., Raleigh, E. A., Mckane, M., Cryderman, D., Bilodeau, P., Mcweeny, K. (1999) Molecular evolution of the Escherichia coli chromosome. V. Recombination patterns among strains of diverse origin. Genetics 153, 539–54.PubMedGoogle Scholar
  22. 22.
    Shen, P., Huang, H. V. (1986) Homologous recombination in Escherichia coli: dependence on substrate length and homology. Genetics 112, 441–57PubMedGoogle Scholar
  23. 23.
    Dykhuizen, D. E., Green, L. (1991) Recombination in Escherichia coli and the definition of biological species. J Bacteriol 173, 7257–68.PubMedGoogle Scholar
  24. 24.
    Milkman, R. (1997) Recombination and population structure in Escherichia coli. Genetics 146, 745–50.PubMedGoogle Scholar
  25. 25.
    Wertz, J. E., Goldstone, C., Gordon, D. M., Riley, M. A. (2003) A molecular phylogeny of enteric bacteria and implications for a bacterial species concept. J Evol Biol 16, 1236–48.CrossRefPubMedGoogle Scholar
  26. 26.
    Maiden, M. C., Bygraves, J. A., Feil, E., Morelli, G., Russell, J. E., Urwin, R., Zhang, Q., Zhou, J., Zurth, K., Caugant, D. A., Feavers, I. M., Achtman, M., Spratt, B. G. (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA 95, 3140–5.CrossRefPubMedGoogle Scholar
  27. 27.
    Feil, E. J., Holmes, E. C., Bessen, D. E., Chan, M. S., Day, N. P., Enright, M. C., Goldstein, R., Hood, D. W., Kalia, A., Moore, C. E., Zhou, J., Spratt, B. G. (2001) Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc Natl Acad Sci USA 98, 182–7.CrossRefPubMedGoogle Scholar
  28. 28.
    Feil, E. J., Maiden, M. C., Achtman, M., Spratt, B. G. (1999) The relative contributions of recombination and mutation to the divergence of clones of Neisseria meningitidis. Mol Biol Evol 16, 1496–502.PubMedGoogle Scholar
  29. 29.
    Feil, E. J., Smith, J. M., Enright, M. C., Spratt, B. G. (2000) Estimating recombinational parameters in Streptococcus pneumoniae from multilocus sequence typing data. Genetics 154, 1439–50.PubMedGoogle Scholar
  30. 30.
    Feil, E. J., Spratt, B. G. (2001) Recombination and the population structures of bacterial pathogens. Annu Rev Microbiol 55, 561–90.CrossRefPubMedGoogle Scholar
  31. 31.
    Hanage, W. P., Fraser, C., Spratt, B. G. (2006) The impact of homologous recombination on the generation of diversity in bacteria. J Theor Biol 239, 210–9.CrossRefPubMedGoogle Scholar
  32. 32.
    Guttman, D. S., Dykhuizen, D. E. (1994) Detecting selective sweeps in naturally occurring Escherichia coli. Genetics 138, 993–1003.Google Scholar
  33. 33.
    Guttman, D. S., Dykhuizen, D. E. (1994) Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science 266, 1380–3.CrossRefPubMedGoogle Scholar
  34. 34.
    Hanage, W. P., Fraser, C., Spratt, B. G. (2005) Fuzzy species among recombinogenic bacteria. BMC Biol 3, 6.CrossRefPubMedGoogle Scholar
  35. 35.
    Hanage, W. P., Fraser, C., Spratt, B. G. (2006) Sequences, sequence clusters and bacterial species. Philos Trans R Soc Lond B Biol Sci 361, 1917–27.CrossRefPubMedGoogle Scholar
  36. 36.
    Roncero, C., Sanderson, K. E., Casadaban, M. J. (1991) Analysis of the host ranges of transposon bacteriophages Mu, MuhP1, and D108 by use of lipopolysaccharide mutants of Salmonella typhimurium LT2. J Bacteriol 173, 5230–3.PubMedGoogle Scholar
  37. 37.
    Papke, R. T., Zhaxybayeva, O., Feil, E. J., Sommerfeld, K., Muise, D., Doolittle, W. F. (2007) Searching for species in haloarchaea. Proc Natl Acad Sci U S A 104, 14092–7.CrossRefPubMedGoogle Scholar
  38. 38.
    Whitaker, R. J., Grogan, D. W., Taylor, J. W. (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301, 976–8.CrossRefPubMedGoogle Scholar
  39. 39.
    Whitaker, R. J., Grogan, D. W., Taylor, J. W. (2005) Recombination shapes the natural population structure of the hyperthermophilic archaeon Sulfolobus islandicus. Mol Biol Evol 22, 2354–61.CrossRefGoogle Scholar
  40. 40.
    Vulic, M., Dionisio, F., Taddei, F., Radman, M. (1997) Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in Enterobacteria. Proc Natl Acad Sci USA 94, 9763–7.CrossRefPubMedGoogle Scholar
  41. 41.
    Vulic, M., Lenski, R. E., Radman, M. (1999) Mutation, recombination, and incipient speciation of bacteria in the laboratory. Proc Natl Acad Sci USA 96, 7348–51.CrossRefPubMedGoogle Scholar
  42. 42.
    Majewski, J., Cohan, F. M. (1999) DNA sequence similarity requirements for interspecific recombination in Bacillus. Genetics 153, 1525–33.PubMedGoogle Scholar
  43. 43.
    Zawadzki, P., Roberts, M. S., Cohan, F. M. (1995) The log-linear relationship between sexual isolation and sequence divergence in Bacillus transformation is robust. Genetics 140, 917–32.PubMedGoogle Scholar
  44. 44.
    Springer, B., Sander, P., Sedlacek, L., Hardt, W. D., Mizrahi, V., Schar, P., Bottger, E. C. (2004) Lack of mismatch correction facilitates genome evolution in mycobacteria. Mol Microbiol 53, 1601–9.CrossRefPubMedGoogle Scholar
  45. 45.
    Matic, I., Rayssiguier, C., Radman, M. (1995) Interspecies gene exchange in bacteria: the role of SOS and mismatch repair systems in evolution of species. Cell 80, 507–15.CrossRefPubMedGoogle Scholar
  46. 46.
    Brown, E. W., Leclerc, J. E., Li, B., Payne, W. L., Cebula, T. A. (2001) Phylogenetic evidence for horizontal transfer of mutS alleles among naturally occurring Escherichia coli strains. J Bacteriol 183, 1631–44.CrossRefPubMedGoogle Scholar
  47. 47.
    Demerec, M., Ohta, N. (1964) Genetic analyses of Salmonella typhimurium X Escherichia coli hybrids. Proc Natl Acad Sci USA 52, 317–23.CrossRefPubMedGoogle Scholar
  48. 48.
    Hanage, W. P., Spratt, B. G., Turner, K. M., Fraser, C. (2006) Modelling bacterial speciation. Philos Trans R Soc Lond B Biol Sci 361, 2039–44.CrossRefPubMedGoogle Scholar
  49. 49.
    Falush, D., Torpdahl, M., Didelot, X., Conrad, D. F., Wilson, D. J., Achtman, M. (2006) Mismatch induced speciation in Salmonella: model and data. Philos Trans R Soc Lond B Biol Sci 361, 2045–53.CrossRefPubMedGoogle Scholar
  50. 50.
    Fraser, C., Hanage, W. P., Spratt, B. G. (2007) Recombination and the nature of bacterial speciation. Science 315, 476–80.CrossRefPubMedGoogle Scholar
  51. 51.
    Gordon, D. M., Bauer, S., Johnson, J. R. (2002) The genetic structure of Escherichia coli populations in primary and secondary habitats. Microbiology 148, 1513–22.PubMedGoogle Scholar
  52. 52.
    Gordon, D. M., Cowling, A. (2003) The distribution and genetic structure of Escherichia coli in Australian vertebrates: host and geographic effects. Microbiology 149, 3575–86.CrossRefPubMedGoogle Scholar
  53. 53.
    Gordon, D. M., Fitzgibbon, F. (1999) The distribution of enteric bacteria from Australian mammals: host and geographical effects. Microbiology 145 (Pt 10), 2663–71.PubMedGoogle Scholar
  54. 54.
    Day, W. A., Jr., Fernandez, R. E., Maurelli, A. T. (2001) Pathoadaptive mutations that enhance virulence: genetic organization of the cadA regions of Shigella spp. Infect Immun 69, 7471–80.CrossRefPubMedGoogle Scholar
  55. 55.
    Nakata, N., Tobe, T., Fukuda, I., Suzuki, T., Komatsu, K., Yoshikawa, M., Sasakawa, C. (1993) The absence of a surface protease, OmpT, determines the intercellular spreading ability of Shigella: the relationship between the ompT and kcpA loci. Mol Microbiol 9, 459–68.CrossRefPubMedGoogle Scholar
  56. 56.
    Maurelli, A. T., Fernández, R. E., Bloch, C. A., Rode, C. K., Fasano, A. (1998) “Black holes” and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli. Proc Natl Acad Sci, USA 95, 3943–8.CrossRefGoogle Scholar
  57. 57.
    May, B. J., Zhang, Q., Li, L. L., Paustian, M. L., Whittam, T. S., Kapur, V. (2001) Complete genomic sequence of Pasteurella multocida, Pm70. Proc Natl Acad Sci, USA 98, 3460–5.CrossRefPubMedGoogle Scholar
  58. 58.
    Lawrence, J. G. (2002) Gene transfer in bacteria: speciation without species? Theor Popul Biol 61, 449–60.CrossRefPubMedGoogle Scholar
  59. 59.
    Sheppard, S. K., Mccarthy, N. D., Falush, D., Maiden, M. C. (2008) Convergence of Campylobacter species: implications for bacterial evolution. Science 320, 237–9.CrossRefPubMedGoogle Scholar
  60. 60.
    Moran, N. A., Munson, M. A., Baumann, P., Ishikawa, H. (1993) A molecular clock in endosymbiotic bacteria is calibrated using insect hosts. Proc R Soc Lond B 253, 167–71.CrossRefGoogle Scholar
  61. 61.
    Ochman, H., Wilson, A. C. (1988) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26, 74–86.CrossRefGoogle Scholar
  62. 62.
    Sharp, P. M., Li, W.-H. (1987) The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias. Mol Biol Evol 4, 222–30.PubMedGoogle Scholar
  63. 63.
    Sharp, P. M., Li, W.-H. (1987) The codon adaptation index – a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15, 1281–95.CrossRefPubMedGoogle Scholar
  64. 64.
    Li, W. H., Wu, C. I., Luo, C. C. (1985) A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 2, 150–74.PubMedGoogle Scholar
  65. 65.
    Li, W. H. (1993) Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 36, 96–9.CrossRefPubMedGoogle Scholar
  66. 66.
    Retchless, A. C., Lawrence, J. G. (2007) Temporal fragmentation of speciation in bacteria. Science 317, 1093–6.CrossRefPubMedGoogle Scholar
  67. 67.
    Ochman, H., Wilson, A. C. (1987) Evolutionary history of enteric bacteria, in Escherichia Coli and Salmonella Typhimurium: Cellular and Molecular Biology (Neidhardt, F. C., Ingraham J. L., Low K. B., Magasanik B., Sch- aechter M., Umbarger H. E., ed.) American Society for Microbiology, Washington, D. C. 1649–54.Google Scholar
  68. 68.
    Lawrence, J. G. (1997) Selfish operons and speciation by gene transfer. Trends Microbiol 5, 355–9.CrossRefPubMedGoogle Scholar
  69. 69.
    Lawrence, J. G. (1999) Gene transfer, speciation, and the evolution of bacterial genomes. Curr Opin Microbiol 2, 519–23.CrossRefPubMedGoogle Scholar
  70. 70.
    Welch, R. A., Burland, V., Plunkett, G., 3rd, Redford, P., Roesch, P., Rasko, D., Buckles, E. L., Liou, S. R., Boutin, A., Hackett, J., Stroud, D., Mayhew, G. F., Rose, D. J., Zhou, S., Schwartz, D. C., Perna, N. T., Mobley, H. L., Donnenberg, M. S., Blattner, F. R. (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci USA 99, 17020–4.CrossRefGoogle Scholar
  71. 71.
    Kudva, I. T., Evans, P. S., Perna, N. T., Barrett, T. J., Ausubel, F. M., Blattner, F. R., Calderwood, S. B. (2002) Strains of Escherichia coli O157:H7 differ primarily by insertions or deletions, not single-nucleotide polymorphisms. J Bacteriol 184, 1873–9.CrossRefPubMedGoogle Scholar
  72. 72.
    Lawrence, J. G., Ochman, H. (1998) Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci USA 95, 9413–7.CrossRefPubMedGoogle Scholar
  73. 73.
    Choi, I. G., Kim, S. H. (2007) Global extent of horizontal gene transfer. Proc Natl Acad Sci USA 104, 4489–94.CrossRefPubMedGoogle Scholar
  74. 74.
    Creevey, C. J., Fitzpatrick, D. A., Philip, G. K., Kinsella, R. J., O’connell, M. J., Pentony, M. M., Travers, S. A., Wilkinson, M., Mcinerney, J. O. (2004) Does a tree-like phylogeny only exist at the tips in the prokaryotes? Proceedings 271, 2551–8.Google Scholar
  75. 75.
    Dagan, T., Martin, W. (2006) The tree of one percent. Genome Biol 7, 118.CrossRefPubMedGoogle Scholar
  76. 76.
    Lawrence, J. G., Hatfull, G. F., Hendrix, R. W. (2002) Imbroglios of viral taxonomy: genetic exchange and failings of phenetic approaches. J Bacteriol 184, 4891–905.CrossRefPubMedGoogle Scholar

Copyright information

© Humana Press, a part of Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Jeffrey G. Lawrence
    • 1
  • Adam C. Retchless
    • 1
  1. 1.Department of Biological SciencesUniversity of PittsburghPittsburghUSA

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