Sexual isolation and speciation in bacteria

  • Frederick M. Cohan
Part of the Contemporary Issues in Genetics and Evolution book series (CIGE, volume 9)


Like organisms from all other walks of life, bacteria are capable of sexual recombination. However, unlike most plants and animals, bacteria recombine only rarely, and when they do they are extremely promiscuous in their choice of sexual partners. There may be no absolute constraints on the evolutionary distances that can be traversed through recombination in the bacterial world, but interspecies recombination is reduced by a variety of factors, including ecological isolation, behavioral isolation, obstacles to DNA entry, restriction endonuclease activity, resistance to integration of divergent DNA sequences, reversal of recombination by mismatch repair, and functional incompatibility of recombined segments. Typically, individual bacterial species are genetically variable for most of these factors. Therefore, natural selection can modulate levels of sexual isolation, to increase the transfer of genes useful to the recipient while minimizing the transfer of harmful genes. Interspecies recombination is optimized when recombination involves short segments that are just long enough to transfer an adaptation, without co-transferring potentially harmful DNA flanking the adaptation. Natural selection has apparently acted to reduce sexual isolation between bacterial species. Evolution of sexual isolation is not a milestone toward speciation in bacteria, since bacterial recombination is too rare to oppose adaptive divergence between incipient species. Ironically, recombination between incipient bacterial species may actually foster the speciation process, by prohibiting one incipient species from out-competing the other to extinction. Interspecific recombination may also foster speciation by introducing novel gene loci from divergent species, allowing invasion of new niches.

Key words

horizontal transfer species concept recombination 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Atwood, K.C., L.K. Schneider & F.J. Ryan, 1951. Periodic selection in Escherichia coli. Proc. Natl. Acad. Sci. USA 37: 146–155.PubMedCrossRefGoogle Scholar
  2. Avise, J.C., 2000. Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, MA.Google Scholar
  3. Bergan, T. & A.K. Vaksvik, 1983. Taxonomic implications of quantitative transformation in Acinetobacter calcoaceticus. Zentralbl. Bakteriol. Mikrobiol. Hyg. [A] 254: 214–228.Google Scholar
  4. Bessen, D.E., J.R. Carapetis, B. Beall, R. Katz, M. Hibble, B.J. Currie, T. Collingridge, M.W. Izzo, D.A. Scaramuzzino & K.S. Sriprakash, 2000. Contrasting molecular epidemiology of group A streptococci causing tropical and nontropical infections of the skin and throat. J. Infect. Dis. 182: 1109–1116.PubMedCrossRefGoogle Scholar
  5. Bickle, T.A. & D.H. Kruger, 1993. Biology of DNA restriction. Microbiol. Rev. 57: 434–450.PubMedGoogle Scholar
  6. Brown, E.W., J.E. LeClerc, B. Li, W.L. Payne & T.A. Cebula, 2001. Phylogenetic evidence for horizontal transfer of mutS alleles among naturally occurring Escherichia coli strains. J. Bacteriol. 183: 1631–1644.PubMedCrossRefGoogle Scholar
  7. Cohan, F.M., 1994. The effects of rare but promiscuous genetic exchange on evolutionary divergence in prokaryotes. Am. Nat. 143: 965–986.CrossRefGoogle Scholar
  8. Cohan, F.M., 2001. Bacterial species and speciation. Syst. Biol. 50: 513–524.PubMedCrossRefGoogle Scholar
  9. Cohan, F.M., 2002. Clonal structure: an overview, pp. 158–161 in Encyclopedia of Evolution, edited by M. Pagel. Oxford University Press, New York.Google Scholar
  10. Cohan, F.M., in press. What are bacterial species? Ann. Rev. Microbiol. 56.Google Scholar
  11. Cohan, F.M., M.S. Roberts & E.C. King, 1991. The potential for genetic exchange by transformation within a natural population of Bacillus subtilis. Evolution 45: 1393–1421.CrossRefGoogle Scholar
  12. Cooper, V.S., D. Schneider, M. Blot & R.E. Lenski, 2001. Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J. Bacteriol. 183: 2834–2841.CrossRefGoogle Scholar
  13. Danner, D.B., H.O. Smith & S.A. Narang, 1982. Construction of DNA recognition sites active in Haemophilus transformation. Proc. Natl. Acad. Sci. USA 79: 2393–2397.PubMedCrossRefGoogle Scholar
  14. Davies, J., 1996. Origins and evolution of antibiotic resistance. Microbiologia 12: 9–16.PubMedGoogle Scholar
  15. de Queiroz, K., 1998. The general lineage concept of species, species criteria, and the process of speciation, in Endless Forms: Species and Speciation, edited by D.J. Howard & S.H. Berlocher. Oxford University Press, Oxford.Google Scholar
  16. Denamur, E., G. Lecointre, P. Darlu, O. Tenaillon, C. Acquaviva, C. Sayada, I. Sunjevaric, R. Rothstein, J. Elion, F. Taddei, M. Radman & I. Matic, 2000. Evolutionary implications of the frequent horizontal transfer of mismatch repair genes. Cell 103: 711–721.PubMedCrossRefGoogle Scholar
  17. Desiere, F., W.M. McShan, D. van Sinderen, J.J. Ferretti & H. Brussow, 2001. Comparative genomics reveals close genetic relationships between phages from dairy bacteria and pathogenic Streptococci: evolutionary implications for prophage-host interactions. Virology 288: 325–341.PubMedCrossRefGoogle Scholar
  18. Dubnau, D., 1991. Genetic competence in Bacillus subtilis. Microbiol. Rev. 55: 395–424.PubMedGoogle Scholar
  19. Dubnau, D., 1999. DNA uptake in bacteria. Annu. Rev. Microbiol. 53: 217–244.PubMedCrossRefGoogle Scholar
  20. Duncan, K.E., C.A. Istock, J.B. Graham & N. Ferguson, 1989. Genetic exchange between Bacillus subtilis and Bacillus licheni-formis: variable hybrid stability and the nature of species. Evolution 43: 1585–1609.CrossRefGoogle Scholar
  21. Feil, E.J., M.C. Maiden, M. Achtman & B.G. Spratt, 1999. The relative contributions of recombination and mutation to the divergence of clones of Neisseria meningitidis. Mol. Biol. Evol. 16:1496–1502.PubMedCrossRefGoogle Scholar
  22. Feil, E.J., M.C. Enright & B.G. Spratt, 2000a. Estimating the relative contributions of mutation and recombination to clonal diversification: a comparison between Neisseria meningitidis and Streptococcus pneumoniae. Res. Microbiol. 151:465–469.PubMedCrossRefGoogle Scholar
  23. Feil, E.J., J.M. Smith, M.C. Enright & B.G. Spratt, 2000b. Estimating recombinational parameters in Streptococcus pneumoniae from multilocus sequence typing data. Genetics 154: 1439–1450.PubMedGoogle Scholar
  24. Giraud, A., I. Matic, O. Tenaillon, A. Clara, M. Radman, M. Fons & F. Taddei, 2001. Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science 291:2606–2608.PubMedCrossRefGoogle Scholar
  25. Goodman, S.D. & J.J. Scocca, 1988. Identification and arrangement of the DNA sequence recognized in specific transformation of Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. USA 85:6982–6986.PubMedCrossRefGoogle Scholar
  26. Groisman, E.A. & H. Ochman, 1997. How Salmonella became a pathogen. Trends Microbiol. 5: 343–349.PubMedCrossRefGoogle Scholar
  27. Guttman, D.S. & D.E. Dykhuizen, 1994. Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science 266: 1380–1383.PubMedCrossRefGoogle Scholar
  28. Haas, R., T.F. Meyer & J.P. van Putten, 1993. Aflagellated mutants of Helicobacter pylori generated by genetic transformation of naturally competent strains using transposon shuttle mutagenesis. Mol. Microbiol. 8:753–760.PubMedCrossRefGoogle Scholar
  29. Hamilton, C.M., M. Aldea, B.K. Washburn, P. Babitzke & S.R. Kushner, 1989. New method for generating deletions and gene replacements in Escherichia coli. J. Bacteriol. 171:4617–4622.PubMedGoogle Scholar
  30. Harris-Warrick, R.M. & J. Lederberg, 1978. Interspecies transformation in Bacillus: sequence heterology as the major barrier. J. Bacteriol. 133:1237–1245.PubMedGoogle Scholar
  31. Hey, J. & J. Wakeley, 1997. A coalescent estimator of the population recombination rate. Genetics 145: 833–846.PubMedGoogle Scholar
  32. Imhof, M. & C Schlotterer, 2001. Fitness effects of advantageous mutations in evolving Escherichia coli populations. Proc. Natl. Acad. Sci. USA 98: 1113–1117.PubMedCrossRefGoogle Scholar
  33. Ippen-Ihler, K., 1989. Bacterial conjugation, in Gene Transfer in the Environment, edited by S.B. Levy & R.V. Levy. McGraw-Hill, New York.Google Scholar
  34. Istock, C.A., J.A. Bell, N. Ferguson & N.L. Istock, 1996. Bacterial species and evolution: theoretical and practical perspectives. J. Ind. Microbiol. 17: 137–150.CrossRefGoogle Scholar
  35. Jain, R., M.C. Rivera & J.A. Lake, 1999. Horizontal gene transfer among genomes: the complexity hypothesis. Proc. Natl. Acad. Sci. USA 96: 3801–3806.PubMedCrossRefGoogle Scholar
  36. Lacks, S.A., S. Ayalew, A.G. de la Campa & B. Greenberg, 2000. Regulation of competence for genetic transformation in Streptococcus pneumoniae: expression of dpnA, a late competence gene encoding a DNA methyltransferase of the DpnIIrestriction system. Mol. Microbiol. 35: 1089–1098.PubMedCrossRefGoogle Scholar
  37. Lawrence, J., 1999. Selfish operons: the evolutionary impact of gene clustering in prokaryotes and eukaryotes. Curr. Opin. Genet. Dev. 9: 642–648.PubMedCrossRefGoogle Scholar
  38. Lawrence, J., 2001. Catalyzing bacterial speciation: correlating lateral transfer with genetic headroom. Syst. Biol. 50: 479–496.PubMedCrossRefGoogle Scholar
  39. LeClerc, J.E., B. Li, W.L. Payne & T.A. Cebula, 1996. High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274: 1208–1211.PubMedCrossRefGoogle Scholar
  40. Leff, L., J. McArthur & L. Shimkets, 1992. Information spiraling: movement of bacteria and their genes in streams. Microb. Ecol. 24: 11–24.CrossRefGoogle Scholar
  41. Lin, L.F., J. Posfai, R.J. Roberts & H. Kong, 2001. Comparative genomics of the restriction-modification systems in Helicobacter pylori. Proc. Natl. Acad. Sci. USA 98: 2740–2745.PubMedCrossRefGoogle Scholar
  42. Lorenz, M.G. & J. Sikorski, 2000. The potential for intraspe-cific horizontal gene exchange by natural genetic transformation: sexual isolation among genomovars of Pseudomonas stutzeri. Microbiology 146(Pt 12): 3081–3090.PubMedGoogle Scholar
  43. Lorenz, M.G. & W. Wackernagel, 1994. Bacterial gene transfer by natural genetic transformation in the environment. Microbiol. Rev. 58: 563–602.PubMedGoogle Scholar
  44. Madigan, M., J. Martinko & J. Parker, 1999. Brock’s Biology of Microorganisms. Prentice-Hall, Upper Saddle River, NJ.Google Scholar
  45. Majewski, J., 2001. Sexual isolation in bacteria. FEMS Microbiol. Lett. 199: 161–169.PubMedCrossRefGoogle Scholar
  46. Majewski, J. & F.M. Cohan, 1998. The effect of mismatch repair and heteroduplex formation on sexual isolation in Bacillus. Genetics 148: 13–18.PubMedGoogle Scholar
  47. Majewski, J. & F.M. Cohan, 1999. DNA sequence similarity requirements for interspecific recombination in Bacillus. Genetics 153: 1525–1533.PubMedGoogle Scholar
  48. Majewski, J., P. Zawadzki, P. Pickerill, F.M. Cohan & C.G. Dowson, 2000. Barriers to genetic exchange between bacterial species: Streptococcus pneumoniae transformation. J. Bacteriol. 182: 1016–1023.PubMedCrossRefGoogle Scholar
  49. Matic, I., F. Taddei & M. Radman, 2000. No genetic barriers between Salmonella enterica serovar typhimurium and Escherichia coli in SOS-induced mismatch repair-deficient cells. J. Bacteriol. 182: 5922–5924.PubMedCrossRefGoogle Scholar
  50. Matic, I., M. Radman, F. Taddei, B. Picard, C. Doit, E. Bingen, E. Denamur & J. Elion, 1997. Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science 277: 1833–1834.PubMedCrossRefGoogle Scholar
  51. Maynard Smith, J., C.G. Dowson & B.G. Spratt, 1991. Localized sex in bacteria. Nature 349: 29–31.CrossRefGoogle Scholar
  52. Maynard Smith, J., N. Smith, M, O’Rourke & B.G. Spratt, 1993. How clonal are bacteria? Proc. Natl. Acad. Sci. USA 90: 4384–4388.CrossRefGoogle Scholar
  53. Mayr, E., 1963. Animal Species and Evolution. Belknap Press of Harvard University Press, Cambridge.Google Scholar
  54. Mazodier, P. & J. Davies, 1991. Gene transfer between distantly related bacteria. Annu. Rev. Genet. 25: 147–171.PubMedCrossRefGoogle Scholar
  55. Miller, R.V., 2001. Environmental bacteriophage-host interactions: factors contribution to natural transduction. Antonie Van Leeuwenhoek 79: 141–147.PubMedCrossRefGoogle Scholar
  56. Moran, N.A. & J.J. Wernegreen, 2000. Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol. Evol. 15: 321–326.PubMedCrossRefGoogle Scholar
  57. Morrison, D.A. & M.S. Lee, 2000. Regulation of competence for genetic transformation in Streptococcus pneumoniae: a link between quorum sensing and DNA processing genes. Res. Microbiol. 151:445–451.PubMedCrossRefGoogle Scholar
  58. Ochman, H., J.G. Lawrence & E.A. Groisman, 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299–304.PubMedCrossRefGoogle Scholar
  59. O’Rourke, M. & B.G. Spratt, 1994. Further evidence for the non-clonal population structure of Neisseria gonorrhoeae: extensive genetic diversity within isolates of the same electrophoretic type. Microbiology 140(Pt 6): 1285–1290.PubMedCrossRefGoogle Scholar
  60. Oliver, A., R. Canton, P. Campo, F. Baquero & J. Blazquez, 2000. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288: 1251–1254.PubMedCrossRefGoogle Scholar
  61. Pozzi, G., L. Masala, F. Iannelli, R. Manganelli, L.S. Havarstein, L. Piccoli, D. Simon & D.A. Morrison, 1996. Competence for genetic transformation in encapsulated strains of Streptococcus pneumoniae: two allelic variants of the peptide pheromone. J. Bacteriol. 178: 6087–6090.PubMedGoogle Scholar
  62. Rainey, P.B. & M. Travisano, 1998. Adaptive radiation in a heterogeneous environment. Nature 394: 69–72.PubMedCrossRefGoogle Scholar
  63. Rayssiguier, C., D.S. Thaler & M. Radman, 1989. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature 342: 396–401.PubMedCrossRefGoogle Scholar
  64. Rivera, M.C., R. Jain, J.E. Moore & J.A. Lake, 1998. Genomic evidence for two functionally distinct gene classes. Proc. Natl. Acad. Sci. USA 95: 6239–6244.PubMedCrossRefGoogle Scholar
  65. Roberts, M.S. & F.M. Cohan, 1993. The effect of DNA sequence divergence on sexual isolation in Bacillus. Genetics 134: 401–408.PubMedGoogle Scholar
  66. Roberts, M.S. & F.M. Cohan, 1995. Recombination and migration rates in natural populations of Bacillus subtilis and Bacillus mojavensis. Evolution 49: 1081–1094.CrossRefGoogle Scholar
  67. Roberts, R.J. & D. Macelis, 1992. Restriction enzymes and their isoschizomers. Nucl. Acids Res. 20: 2167–2180.PubMedGoogle Scholar
  68. Rocha, E.P., A. Danchin & A. Viari, 2001. Evolutionary role of restriction/modification systems as revealed by comparative genome analysis. Genome Res. 11: 946–958.PubMedCrossRefGoogle Scholar
  69. Schofield, M.J., S. Nayak, T.H. Scott, C. Du & P. Hsieh, 2001. Interaction of Escherichia coli MutS and MutL at a DNA mismatch. J. Biol. Chem. 276: 28291–28299.PubMedCrossRefGoogle Scholar
  70. Schubert, S., A. Rakin, H. Karch, E. Carniel & J. Heesemann, 1998. Prevalence of the high-pathogenicity island of Yersinia species among Escherichia coli strains that are pathogenic to humans. Infect. Immun. 66: 480–485.PubMedGoogle Scholar
  71. Sekizaki, T., M. Osaki, D. Takamatsu & Y. Shimoji, 2001. Distribution of the SsuDAT1I restriction-modification system among different serotypes of Streptococcus suis. J. Bacteriol. 183: 5436–5440.PubMedCrossRefGoogle Scholar
  72. Selander, R. & J. Musser, 1990. Population genetics of bacterial pathogenesis, pp. 11–36 in Molecular Basis of Bacterial Pathogenesis, edited by B. Iglewski & V. Clark. Academic Press, San Diego.Google Scholar
  73. Sharp, P.M. & W.H. Li, 1986. An evolutionary perspective on synonymous codon usage in unicellular organisms. J. Mol. Evol. 24: 28–38.PubMedCrossRefGoogle Scholar
  74. Shoemaker, N.B., H. Vlamakis, K. Hayes & A.A. Salyers, 2001. Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon. Appl. Environ. Microbiol. 67: 561–568.PubMedCrossRefGoogle Scholar
  75. Sikorski, J., N. Teschner & W. Wackernagel, 2002. Highly different levels of natural transformation are associated with genomic subgroups within a local population of Pseudomonas stutzeri from soil. Appl. Environ. Microbiol. 68: 865–873.PubMedCrossRefGoogle Scholar
  76. Sniegowski, P.D., P.J. Gerrish & R.E. Lenski, 1997. Evolution of high mutation rates in experimental populations of E. coli. Nature 387: 703–705.PubMedCrossRefGoogle Scholar
  77. Sokurenko, E.V., D.L. Hasty & D.E. Dykhuizen, 1999. Pathoad-aptive mutations: gene loss and variation in bacterial pathogens. Trends Microbiol. 7: 191–195.PubMedCrossRefGoogle Scholar
  78. Sparling, P.F., 1966. Genetic transformation of Neisseria gonorrhoeae to streptomycin resistance. J. Bacteriol. 92: 1364–1371.PubMedGoogle Scholar
  79. Spratt, B.G., L.D. Bowler, Q.Y. Zhang, J. Zhou & J.M. Smith, 1992. Role of interspecies transfer of chromosomal genes in the evolution of penicillin resistance in pathogenic and commensal Neisseria species. J. Mol. Evol. 34: 115–125.PubMedCrossRefGoogle Scholar
  80. Stotzky, G., 1989. Gene transfer among bacteria in soil, pp. 165–222 in Gene Transfer in the Environment, edited by S.B.L.a.R.V Miller. McGraw-Hill, New York.Google Scholar
  81. Suerbaum, S., J. Maynard Smith, K. Bapumia, G. Morelli, N. Smith, E. Kunstmann, I. Dyrek & M. Achtman, 1998. Free recombination within Helicobacter pylori. Proc. Natl. Acad. Sci. USA 95: 12619–12624.PubMedCrossRefGoogle Scholar
  82. Tortosa, P., L. Logsdon, B. Kraigher, Y. Itoh, I. Mandic-Mulec & D. Dubnau, 2001. Specificity and genetic polymorphism of the Bacillus competence quorum-sensing system. J. Bacteriol. 183: 451–460.PubMedCrossRefGoogle Scholar
  83. Treves, D.S., S. Manning & J. Adams, 1998. Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol. Biol. Evol. 15: 789–797.PubMedCrossRefGoogle Scholar
  84. Van Spanning, R.J., W.N. Reijnders & A.H. Stouthamer, 1995. Integration of heterologous DNA into the genome of Paracoccus denitrificans is mediated by a family of IS1248-related elements and a second type of integrative recombination event. J. Bacteriol. 177: 4772–4778.PubMedGoogle Scholar
  85. Vulic, M., F. Dionisio, F. Taddei & M. Radman, 1997. Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in enterobacteria. Proc. Natl. Acad. Sci. USA 94: 9763–9767.PubMedCrossRefGoogle Scholar
  86. Wiley, E., 1978. The evolutionary species concept reconsidered. Syst. Zool. 27: 17–26.CrossRefGoogle Scholar
  87. Zawadzki, P. & F.M. Cohan, 1995. The size and continuity of DNA segments integrated in Bacillus transformation. Genetics 141: 1231–1243.PubMedGoogle Scholar
  88. Zawadzki, P., M.S. Roberts & F.M. Cohan, 1995. The log-linear relationship between sexual isolation and sequence divergence in Bacillus transformation is robust. Genetics 140: 917–932.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2002

Authors and Affiliations

  • Frederick M. Cohan
    • 1
  1. 1.Department of BiologyWesleyan UniversityMiddletownUSA

Personalised recommendations