Population Genomics and the Bacterial Species Concept

  • Margaret A. Riley
  • Michelle Lizotte-Waniewski
Part of the Methods in Molecular Biology book series (MIMB, volume 532)


In recent years, the importance of horizontal gene transfer (HGT) in bacterial evolution has been elevated to such a degree that many bacteriologists now question the very existence of bacterial species. If gene transfer is as rampant as comparative genomic studies have suggested, how could bacterial species survive such genomic fluidity? And yet, most bacteriologists recognize, and name, as species, clusters of bacterial isolates that share complex phenotypic properties. The Core Genome Hypothesis (CGH) has been proposed to explain this apparent paradox of fluid bacterial genomes associated with stable phenotypic clusters. It posits that there is a core of genes responsible for maintaining the species-specific phenotypic clusters observed throughout bacterial diversity and argues that, even in the face of substantial genomic fluidity, bacterial species can be rationally identified and named.


Bacterial species concept core genome hypothesis population genomics 


  1. 1.
    Fox, G. E., Stackebrandt, E., Hespell, R. B., Gibson, J., Maniloff, J., Dyer, T. A., Wolfe, R. S., Balch, W. E., Tanner, R. S., Magrum, L. J., Zablen, L. B., Blakemore, R., Gupta, R., Bonen, L., Lewis, B. J., Stahl, D. A., Luehrsen, K. R., Chen, K. N., Woese, C. R. (1980) The phylogeny of prokaryotes. Science 209, 457–63.CrossRefPubMedGoogle Scholar
  2. 2.
    Olsen, G. J., Woese, C. J. (1993) Ribosomal RNA: a key to phylogeny. FASEB J 7, 113–23.PubMedGoogle Scholar
  3. 3.
    Pace, N. R., Stahl, D. A., Lane, D. J., Olsen, G. J. (1985) Analyzing natural microbial populations by rRNA sequences. ASM News 51, 4–12.Google Scholar
  4. 4.
    Woese, C. R. (1987) Bacterial evolution. Microbiological Reviews 51, 221–71.PubMedGoogle Scholar
  5. 5.
    Woese, C., Kandler, O., Wheelis, M. (1990) Towards a natural system of organisms – proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A 87, 4576–9.CrossRefPubMedGoogle Scholar
  6. 6.
    Ludwig, W., Neumaier, J., Klugbauer, N., Brockmann, E., Roller, C., Jilg, S., Reetz, K., Schachtner, I., Ludvigsen, A., Bachleitner, M., Fischer, U., Schleifer, K., H. (1993) Phylogenetic relationships of Bacteria based on comparative sequence analysis of elongation factor Tu and ATP-synthase beta-subunit genes. Antonie Van Leeuwenhoek 64, 285–305.CrossRefPubMedGoogle Scholar
  7. 7.
    Brown, J., Douady, C., Italia, M., Marshall, W., Stanhope, M. (2001) Universal trees based on large combined protein sequence data sets. Nat Genet 28, 281–5.CrossRefPubMedGoogle Scholar
  8. 8.
    Kidwell, M. (1993) Lateral transfer in natural populations of eukaryotes. Ann Rev Genetics 27, 235–56.CrossRefGoogle Scholar
  9. 9.
    Nelson, K., Selander, R. K. (1994) Intergeneric transfer and recombination of the 6-phosphogluconate dehydrogenase gene (gnd) in enteric bacteria. Proc Natl Acad Sci U S A 91, 10227–31.CrossRefPubMedGoogle Scholar
  10. 10.
    Brown, J. R., Doolittle, W. F. (1997) Archaea and the prokaryote-to-eukaryote transition. Microbiol Mol Biol Rev 61, 456–502.PubMedGoogle Scholar
  11. 11.
    Nesbo, C. L., L’Haridon, S., Stetter, K. O., Doolittle, W. F. (2001) Phylogenetic analyses of two “Archaeal” genes in thermotoga maritima reveal multiple transfers between Archaea and Bacteria. Mol Biol Evol 18, 362–75.PubMedGoogle Scholar
  12. 12.
    Doolittle, W. F. (1999) Lateral genomics. Trends Cell Biol 9, M5–8.CrossRefPubMedGoogle Scholar
  13. 13.
    Doolittle, W. F., Papke, R. T. (2006) Genomics and the bacterial species problem. Genome Biology 7, 116.CrossRefPubMedGoogle Scholar
  14. 14.
    Cohan, F. (2002) What are bacterial species? Annu Rev Microbiol 56, 457–87.CrossRefPubMedGoogle Scholar
  15. 15.
    Sapp, J. (2005) Microbial phylogeny and evolution: Concepts and controversies. The Bacteriums Place in Nature. Oxford University Press, New York.Google Scholar
  16. 16.
    Rossello-Mora, R., Amann, R. (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25, 39–67.CrossRefPubMedGoogle Scholar
  17. 17.
    Shute, L.A., Gutteridge, C.S., Norris, J.R., Berkeley, R.C. (1984) Curie-point pyrolysis mass spectrometry applied to characterization and identification of selected Bacillus species. J Gen Microbiol 130, 343–55.PubMedGoogle Scholar
  18. 18.
    Sneath, P., Stevens, M. (1985) A numerical taxonomic study of Actinobacillus, Pasteurella, and Yersinia. J Gen Microbiol 131, 2711–38.PubMedGoogle Scholar
  19. 19.
    Barrett, S., Sneath, P. (1994) A numerical phenotypic taxonomic study of the genus Neisseria. Microbiology 140, 2867–91.CrossRefPubMedGoogle Scholar
  20. 20.
    Mauchline, W., Keevil, C. (1991) Development of the BIOLOG substrate utilization system for identification of Legionella spp. Appl Environ Microbiol 57, 3345–9.PubMedGoogle Scholar
  21. 21.
    Kirschner, C., Maquelin, K., Pina, P., Thi, N. N., Choo-Smith, L., Sockalingum, G., Sandt, C., Ami, D., Orsini, F., Doglia, S., Allouch, P., Mainfait, M., Puppels, G., Naumann, D. (2001) Classification and identification of enterococci: A comparative phenotypic, genotypic, and vibrational spectroscopic study. J Clin Microbiol 39, 1763–70.CrossRefPubMedGoogle Scholar
  22. 22.
    Cohan, F. (2002) Sexual isolation and speciation in bacteria. Genetica 116, 359–70.CrossRefPubMedGoogle Scholar
  23. 23.
    Godoy, A. P., Ribeiro, M. L., Benvengo, Y. H., Vitiello, L., Miranda M. de C., Mendonca, S., Pedrazzoli, J., Jr (2003) Analysis of antimicrobial susceptibility and virulence factors in Helicobacter pylori clinical isolates. BMC Gastroenterol 3, 20–26.CrossRefPubMedGoogle Scholar
  24. 24.
    Hanage, W. P., Fraser, C., Spratt, B. G. (2005) Fuzzy species among recombinogenic bacteria. BMC Biol 3, 6.CrossRefPubMedGoogle Scholar
  25. 25.
    Priest, F., Barker, M., Baillie, L., Holmes, E., Maiden, M. (2004) Population structure and evolution of the Bacillus cereus group. J Bacteriol 186, 7959–70.CrossRefPubMedGoogle Scholar
  26. 26.
    Thompson, J., Pacocha, S., Pharino, C., Klepac-Ceraj, V., Hunt, D., Benoit, J., Sarma-Rupavtarm, R., Distel, D., Polz, M. (2005) Genotypic diversity within a natural coastal bacterioplankton population. Science 307, 1311–3.CrossRefPubMedGoogle Scholar
  27. 27.
    Baldwin, A., Mahenthiralingam, E., Thickett, K., Honeybourne, D., Maiden, M., Govan, J., Speert, D., Lipuma, J., Vandamme, P., Dowson, C. (2005) Multilocus sequence typing scheme that provides both species and strain differentiation for the Burkholderia cepacia complex. J Clin Microbiol 43, 4665–73.CrossRefPubMedGoogle Scholar
  28. 28.
    Hanage, W., Kaijalainen, T., Syrjanen, R., Auranen, K., Leinonen, M., Makela, P., Spratt, B. (2005) Invasiveness of serotypes and clones of Streptococcus pneumoniae among children in Finland. Infect Immun 73, 431–5.CrossRefPubMedGoogle Scholar
  29. 29.
    Stackebrandt, E., Frederiksen. W., Garrity G. M., Grimont P. A., Kô mpfer P., Maiden M. C., Nesme X., Rossellö -Mora R., Swings J., Trü per H.G., Vauterin L., Ward A. C., Whitman W. B. (2002) Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52, 1043–7.CrossRefPubMedGoogle Scholar
  30. 30.
    Lindh, J., Terenius, O., Faye, I. (2005) 16S rRNA gene-based identification of midgut bacteria from field-caught Anopheles gambiae sensu lato and A. funestus mosquitoes reveals new species related to known insect symbionts. Appl Environ Microbiol 71, 7217–23.CrossRefPubMedGoogle Scholar
  31. 31.
    Drancourt, M., Berger, P., Raoult, D. (2004) Systematic 16S rRNA gene sequencing of atypical clinical isolates identified 27 new bacterial species associated with humans. J Clin Microbiol 42, 2197–202.CrossRefPubMedGoogle Scholar
  32. 32.
    Clarridge, J. R. (2004) Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clin Microbiol Rev 17, 840–62.CrossRefPubMedGoogle Scholar
  33. 33.
    Clayton, R., Sutton, G., Hinkle, P. J., Bult, C., Fields, C. (1995) Intraspecific variation in small-subunit rRNA sequences in GenBank: why single sequences may not adequately represent prokaryotic taxa. Int J Syst Bacteriol 45, 595–9.CrossRefPubMedGoogle Scholar
  34. 34.
    Wertz, J. E., Valletta-Goldstone, C. M., 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
  35. 35.
    Gordon, D. M., Fitzgibbon, F. (1999) The distribution of enteric bacteria from Australian mammals: Host and geographical effects. Microbiology 145, 2663–71.PubMedGoogle Scholar
  36. 36.
    Holt, J. G. (1994) Bergey’s Manual of Determinative Bacteriology, Williams and Wilkins, Baltimore, MD.Google Scholar
  37. 37.
    Maiden, M. (1998) Horizontal genetic exchange, evolution and spread of antibiotic resistance in bacteria. Clin Infect Dis 27, S12–20.CrossRefPubMedGoogle Scholar
  38. 38.
    Feil, E. J., Cooper. J. E, Grundmann, H., Robinson, D. A., Enright, M. C., Berendt, T., Peacock, S. J., Smith, J. M., Murphy, M., Spratt, B. G., Moore, C. E., Day, N. P. (2003) How clonal is Staphylococcus aureus? J Bacteriol 185, 3307–16.CrossRefPubMedGoogle Scholar
  39. 39.
    Whitaker, R., Grogan, D., Taylor, J. (2005) Recombination shapes the natural population structure of the hyperthermophilic archaeon Sulfolobus islandicus. Mol Biol Evol 22, 2354–61.CrossRefPubMedGoogle Scholar
  40. 40.
    Woodward, M., Sojka, M., Sprigings, K., Humphrey, T. (2000) The role of SEF14 and SEF17 fimbriae in the adherence of Salmonella enterica serotype Enteritidis to inanimate surfaces. J Med Microbiol 49, 481–7.PubMedGoogle Scholar
  41. 41.
    Glasner, J., Perna, N. (2004) Comparative genomics of E. coli. Microbiol Today 31.Google Scholar
  42. 42.
    Mau, B., Glasner, J., Darling, A., Perna, N. (2006) Genome-wide detection and analysis of homologous recombination among sequenced strains of Escherichia coli. Genome Biology 7, R44.CrossRefPubMedGoogle Scholar
  43. 43.
    Milkman, R., Raleigh, E., McKanea, M., Crydermanc, 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
  44. 44.
    Milkman, R., Jaeger, E., Mcbride, R. (2003) Molecular evolution of the Escherichia coli chromosome. VI. Two regions of high effective recombination. Genetics 163, 475–83.PubMedGoogle Scholar
  45. 45.
    Edwards, S. V., Fertil, B., Giron, A., Deschavanne, P. J. (2002) A genomic schism in birds revealed by phylogenetic analysis of DNA strings. Systematic Biology 51, 599–613.CrossRefPubMedGoogle Scholar
  46. 46.
    Juhas, M., Power, P. M., Harding, R. M., Ferguson, D. J., Dimopoulou, I. D., Elamin, A. R., Mohd-Zain, Z., Hood, D. W., Adegbola, R., Erwin, A., Smith, A., Munson, R. S., Jr, Harrison, A., Mansfield, L., Bentley, S., Crook, D. W. (2007) Sequence and functional analyses of Haemophilus spp. genomic islands. Genome Biol 8, R237.CrossRefPubMedGoogle Scholar
  47. 47.
    Coleman, M., Sullivan, M., Martiny, A., Steglich, C., Barry, K., Delong, E., Chisholm, S. (2006) Genomic islands and the ecology and evolution of Prochlorococcus. Science 311, 1768–9.CrossRefPubMedGoogle Scholar
  48. 48.
    Waterfield, N., Daborn, P., Dowling, A., Yang, G., Hares, M., Ffrench-Constant, R. (2003) The insecticidal toxin makes caterpillars floppy 2 (Mcf2) shows similarity to HrmA, an avirulence protein from a plant pathogen. FEMS Microbiol Lett 229, 265–70.CrossRefPubMedGoogle Scholar
  49. 49.
    Lan, R., Reeves, P. R. (1996) Gene transfer is a major factor in bacterial evolution. Mol Biol Evol 13, 47–55.PubMedGoogle Scholar
  50. 50.
    Feil, E. (2004) Small change: Keeping pace with microevolution. Nat Rev Microbiol 2, 483–95.CrossRefPubMedGoogle Scholar
  51. 51.
    Dobrindt, U., Reidl, J. (2000) Pathogenicity islands and phage conversion: Evolutionary aspects of bacterial pathogenesis. Int J Med Microbiol 290, 519–27.PubMedGoogle Scholar
  52. 52.
    Karlin, S. (2001) Detecting anomalous gene clusters and pathogenicity islands in diverse bacterial genomes. Trends Microbiol 9, 335–43.CrossRefPubMedGoogle Scholar
  53. 53.
    White, P. A., Mciver, C. J., Rawlinson, W. D. (2001) Integrons and gene cassettes in the Enterobacteriaceae. Antimicrob Agents Chemother 45, 2658–61.CrossRefPubMedGoogle Scholar
  54. 54.
    Godoy, A., Ribeiro, M., Benvengo, Y., Vitiello, L., Miranda, C. M., Mendonca, S., Pedrazzoli, J. J. (2003) Analysis of antimicrobial susceptibility and virulence factors in Helicobacter pylori clinical isolates. BMC Gastroenterol 3, 20.CrossRefPubMedGoogle Scholar
  55. 55.
    Medini, D., Donati, C., Tettelin, H., Masignani, V., Rappuoli, R. (2005) The microbial pan-genome. Curr Opin Genet Dev 15, 589–94.CrossRefPubMedGoogle Scholar
  56. 56.
    Tettelin, H., Masignani, V., Ciesiewicz, M., Donati, C., Medini, D., Ward, N., Angiuli, S., Crabtree, J., Jones, A., Durkin, A. (2005) Genome analysis of multiple pathogenic isolates of Streptoccocus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci USA 102, 13950–5.CrossRefPubMedGoogle Scholar
  57. 57.
    Mayr, E. (1942) Systematics and the Origin of Species, Columbia University Press, New York.Google Scholar
  58. 58.
    Kimura, M. (1968) Genetic variability maintained in a finite population due to mutation production of neutral and nearly neutral isoalleles. Genetic Res Camb 11, 247–69.CrossRefGoogle Scholar
  59. 59.
    Fay, J., Wyckoff, G., Wu, C. (2002) Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature 415, 1024–6.CrossRefPubMedGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Margaret A. Riley
    • 1
  • Michelle Lizotte-Waniewski
    • 1
  1. 1.Department of BiologyUniversity of MassachusettsAmherstUSA

Personalised recommendations