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

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Horizontal Gene Transfer

Part of the book series: Methods in Molecular Biology ((MIMB,volume 532))

Abstract

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.

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References

  1. Aristotle (1910) Historia Animalium (translated by D’Arcy Wentworth Thompson), Clarendon Press, Oxford.

    Google Scholar 

  2. Linnaeus, C. (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis, Holmiae.

    Google Scholar 

  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. 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. 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. 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.

    Article  CAS  PubMed  Google Scholar 

  7. Mayr, E. (1942) Systematics and the Origin of Species, Columbia University Press, New York.

    Google Scholar 

  8. Mayr, E. (1963) Animal Species and Evolution, Harvard University Press, Cambridge.

    Google Scholar 

  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. Van Valen, L. (1976) Ecological species, multispecies, and oaks. Taxon 25, 223–39.

    Article  Google Scholar 

  11. Wiley, E. O. (1978) The evolutionary species concept reconsidered. Syst Zool 27, 17–26.

    Article  Google Scholar 

  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. Levin, B. R. (1981) Periodic selection, infectious gene exchange and the genetic structure of E. coli populations. Genetics 99, 1–23.

    CAS  PubMed  Google Scholar 

  14. Atwood, K. C., Schneider, L. K., Ryan, F. J. (1951) Periodic selection in Escherichia coli. Proc Natl Acad Sci USA 37, 146–55.

    Article  CAS  PubMed  Google Scholar 

  15. Cohan, F. M. (2001) Bacterial species and speciation. Syst Biol 50, 513–24.

    Article  CAS  PubMed  Google Scholar 

  16. Cohan, F. M., Perry, E. B. (2007) A systematics for discovering the fundamental units of bacterial diversity. Curr Biol 17, R373–86.

    Article  CAS  PubMed  Google Scholar 

  17. Ochman, H., Lawrence, J. G., Groisman, E. (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299–304.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  22. Shen, P., Huang, H. V. (1986) Homologous recombination in Escherichia coli: dependence on substrate length and homology. Genetics 112, 441–57

    CAS  PubMed  Google Scholar 

  23. Dykhuizen, D. E., Green, L. (1991) Recombination in Escherichia coli and the definition of biological species. J Bacteriol 173, 7257–68.

    CAS  PubMed  Google Scholar 

  24. Milkman, R. (1997) Recombination and population structure in Escherichia coli. Genetics 146, 745–50.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  30. Feil, E. J., Spratt, B. G. (2001) Recombination and the population structures of bacterial pathogens. Annu Rev Microbiol 55, 561–90.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  32. Guttman, D. S., Dykhuizen, D. E. (1994) Detecting selective sweeps in naturally occurring Escherichia coli. Genetics 138, 993–1003.

    CAS  Google Scholar 

  33. Guttman, D. S., Dykhuizen, D. E. (1994) Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science 266, 1380–3.

    Article  CAS  PubMed  Google Scholar 

  34. Hanage, W. P., Fraser, C., Spratt, B. G. (2005) Fuzzy species among recombinogenic bacteria. BMC Biol 3, 6.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  38. Whitaker, R. J., Grogan, D. W., Taylor, J. W. (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301, 976–8.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  42. Majewski, J., Cohan, F. M. (1999) DNA sequence similarity requirements for interspecific recombination in Bacillus. Genetics 153, 1525–33.

    CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  47. Demerec, M., Ohta, N. (1964) Genetic analyses of Salmonella typhimurium X Escherichia coli hybrids. Proc Natl Acad Sci USA 52, 317–23.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  50. Fraser, C., Hanage, W. P., Spratt, B. G. (2007) Recombination and the nature of bacterial speciation. Science 315, 476–80.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  58. Lawrence, J. G. (2002) Gene transfer in bacteria: speciation without species? Theor Popul Biol 61, 449–60.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  65. Li, W. H. (1993) Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 36, 96–9.

    Article  CAS  PubMed  Google Scholar 

  66. Retchless, A. C., Lawrence, J. G. (2007) Temporal fragmentation of speciation in bacteria. Science 317, 1093–6.

    Article  CAS  PubMed  Google Scholar 

  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. Lawrence, J. G. (1997) Selfish operons and speciation by gene transfer. Trends Microbiol 5, 355–9.

    Article  CAS  PubMed  Google Scholar 

  69. Lawrence, J. G. (1999) Gene transfer, speciation, and the evolution of bacterial genomes. Curr Opin Microbiol 2, 519–23.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  72. Lawrence, J. G., Ochman, H. (1998) Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci USA 95, 9413–7.

    Article  CAS  PubMed  Google Scholar 

  73. Choi, I. G., Kim, S. H. (2007) Global extent of horizontal gene transfer. Proc Natl Acad Sci USA 104, 4489–94.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  Google Scholar 

  75. Dagan, T., Martin, W. (2006) The tree of one percent. Genome Biol 7, 118.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

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Lawrence, J.G., Retchless, A.C. (2009). The Interplay of Homologous Recombination and Horizontal Gene Transfer in Bacterial Speciation. In: Gogarten, M.B., Gogarten, J.P., Olendzenski, L.C. (eds) Horizontal Gene Transfer. Methods in Molecular Biology, vol 532. Humana Press. https://doi.org/10.1007/978-1-60327-853-9_3

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  • DOI: https://doi.org/10.1007/978-1-60327-853-9_3

  • Publisher Name: Humana Press

  • Print ISBN: 978-1-60327-852-2

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