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  • Review Article
  • Published:

The population genetics of commensal Escherichia coli

Nature Reviews Microbiology volume 8, pages 207–217 (2010)Cite this article

Subjects

Key Points

  • Escherichia coli is, paradoxically, both the most frequent commensal aero-anaerobic Gram-negative bacillus of the vertebrate gut and one of the main pathogens, being responsible for both intraintestinal and extraintestinal infections. Deciphering the ecological and evolutionary forces that shape the population structure of the commensal strains will help to understand the emergence of virulence in the species.

  • In the past few decades, successive molecular methods have contributed to the refinement of the clonal concept of E. coli, including serotyping and multilocus enzyme electrophoresis, followed by DNA marker analysis and nucleotide sequencing. Recently, whole-genome sequencing has revealed the organization of the genome and solved the contradiction between the occurence of recombination events and the observed clonality of the species, allowing the reconstruction of a robust phylogenetic history.

  • In parallel, population genetics-based epidemiology has shown that in a single individual there are predominant strains and also resident and transient strains. Clones, which are characterised by their phylogenetic group, are distributed according to environmental factors and the diet, gut morphology and body mass of their hosts.

  • Finally, the relationships between commensalism and virulence have been clarified. The coincidental hypothesis proposes that 'virulence factors' and their change in prevalence among hosts may reflect some local adaptation to commensal habitats rather than virulence per se. Likewise, intestinal microbiota has been shown to play an important part in the emergence of antibiotic resistance.

  • In the future, with the arrival of next-generation sequencing technology, the study of complete genomes of numerous isolates will allow the development of 'population genomics', and metagenomics approaches will take into account the vast accompanying intestinal microbiota that has been largely ignored in defining the commensal niche of E. coli.

Abstract

The primary habitat of Escherichia coli is the vertebrate gut, where it is the predominant aerobic organism, living in symbiosis with its host. Despite the occurrence of recombination events, the population structure is predominantly clonal, allowing the delineation of major phylogenetic groups. The genetic structure of commensal E. coli is shaped by multiple host and environmental factors, and the determinants involved in the virulence of the bacteria may in fact reflect adaptation to commensal habitats. A better characterization of the commensal niche is necessary to understand how a useful commensal can become a harmful pathogen. In this Review we describe the population structure of commensal E. coli, the factors involved in the spread of different strains, how the bacteria can adapt to different niches and how a commensal lifestyle can evolve into a pathogenic one.

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Figure 1: Escherichia coli core genome and pan-genome evolution according to the number of sequenced genomes.
Figure 2: Phylogenetic reconstruction and recombination.
Figure 3: Phylogenetic history of Escherichia coli.

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References

  1. Hobman, J. L., Penn, C. W. & Pallen, M. J. Laboratory strains of Escherichia coli: model citizens or deceitful delinquents growing old disgracefully? Mol. Microbiol. 64, 881–885 (2007).

    Article  CAS  PubMed  Google Scholar 

  2. Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: the unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Kosek, M., Bern, C. & Guerrant, R. L. The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull. World Health Organ. 81, 197–204 (2003).

    PubMed  PubMed Central  Google Scholar 

  4. Russo, T. A. & Johnson, J. R. Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect. 5, 449–456 (2003).

    Article  PubMed  Google Scholar 

  5. Pinheiro da Silva, F. et al. CD16 promotes Escherichia coli sepsis through an FcRγ inhibitory pathway that prevents phagocytosis and facilitates inflammation. Nature Med. 13, 1368–1374 (2007).

    Article  CAS  PubMed  Google Scholar 

  6. Berg, R. D. The indigenous gastrointestinal microflora. Trends Microbiol. 4, 430–435 (1996).

    Article  CAS  PubMed  Google Scholar 

  7. Gordon, D. M. & Cowling, A. The distribution and genetic structure of Escherichia coli in Australian vertebrates: host and geographic effects. Microbiology 149, 3575–3586 (2003). A key study of 2,300 non-domesticated vertebrate hosts, describing the commensal E. coli population structure and identifying some of the forces that shape it.

    Article  CAS  PubMed  Google Scholar 

  8. Savageau, M. A. Escherichia coli habitats, cell types, and molecular mechanisms of gene control. Am. Nat. 122, 732–744 (1983).

    Article  CAS  Google Scholar 

  9. Solo-Gabriele, H. M., Wolfert, M. A., Desmarais, T. R. & Palmer, C. J. Sources of Escherichia coli in a coastal subtropical environment. Appl. Environ. Microbiol. 66, 230–237 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Power, M. L., Littlefield-Wyer, J., Gordon, D. M., Veal, D. A. & Slade, M. B. Phenotypic and genotypic characterization of encapsulated Escherichia coli isolated from blooms in two Australian lakes. Environ. Microbiol. 7, 631–640 (2005).

    Article  CAS  PubMed  Google Scholar 

  11. Mitsuoka, T. & Hayakawa, K. The fecal flora of man. I. Communication: the composition of the fecal flora of different age groups. Zentralbl. Bakteriol. Orig. A. 223, 333–342 (1972).

    Google Scholar 

  12. Penders, J. et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118, 511–521 (2006).

    Article  PubMed  Google Scholar 

  13. Slanetz, L. W. & Bartley, C. H. Numbers of enterococci in water, sewage, and feces determined by the membrane filter technique with an improved medium. J. Bacteriol. 74, 591–595 (1957).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Poulsen, L. K. et al. Spatial distribution of Escherichia coli in the mouse large intestine inferred from rRNA in situ hybridization. Infect. Immun. 62, 5191–5194 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Freter, R., Brickner, H., Fekete, J., Vickerman, M. M. & Carey, K. E. Survival and implantation of Escherichia coli in the intestinal tract. Infect. Immun. 39, 686–703 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Chang, D. E. et al. Carbon nutrition of Escherichia coli in the mouse intestine. Proc. Natl Acad. Sci. USA 101, 7427–7432 (2004). A very convincing study using E. coli mutants in a mouse model of intestinal colonization, showing the nutritional requirements of E. coli in its natural primary habitat.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Peekhaus, N. & Conway, T. What's for dinner?: Entner-Doudoroff metabolism in Escherichia coli. J. Bacteriol. 180, 3495–3502 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Jones, S. A. et al. Respiration of Escherichia coli in the mouse intestine. Infect. Immun. 75, 4891–4899 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Licht, T. R., Tolker-Nielsen, T., Holmstrom, K., Krogfelt, K. A. & Molin, S. Inhibition of Escherichia coli precursor-16S rRNA processing by mouse intestinal contents. Environ. Microbiol. 1, 23–32 (1999).

    Article  CAS  PubMed  Google Scholar 

  20. Rang, C. U. et al. Estimation of growth rates of Escherichia coli BJ4 in streptomycin-treated and previously germfree mice by in situ rRNA hybridization. Clin. Diagn. Lab. Immunol. 6, 434–436 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Syed, S. A., Abrams, G. D. & Freter, R. Efficiency of various intestinal bacteria in assuming normal functions of enteric flora after association with germ-free mice. Infect. Immun. 2, 376–386 (1970).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Bettelheim, K. A. & Lennox-King, S. M. The acquisition of Escherichia coli by new-born babies. Infection 4, 174–179 (1976).

    Article  CAS  PubMed  Google Scholar 

  23. Nowrouzian, F. et al. Escherichia coli in infants' intestinal microflora: colonization rate, strain turnover, and virulence gene carriage. Pediatr. Res. 54, 8–14 (2003).

    Article  CAS  PubMed  Google Scholar 

  24. Jaureguy, F. et al. Effects of intrapartum penicillin prophylaxis on intestinal bacterial colonization in infants. J. Clin. Microbiol. 42, 5184–5188 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Conway, T., Krogfelt, K. A. & Cohen, P. S. The life of commensal Escherichia coli in the mammalian intestine. EcoSal [online] (2004).

    Google Scholar 

  26. Rastegar Lari, A., Gold, F., Borderon, J. C., Laugier, J. & Lafont, J. P. Implantation and in vivo antagonistic effects of antibiotic-susceptible Escherichia coli strains administered to premature newborns. Biol. Neonate 58, 73–78 (1990).

    Article  CAS  PubMed  Google Scholar 

  27. Vollaard, E. J. & Clasener, H. A. Colonization resistance. Antimicrob. Agents Chemother. 38, 409–414 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hudault, S., Guignot, J. & Servin, A. L. Escherichia coli strains colonising the gastrointestinal tract protect germfree mice against Salmonella typhimurium infection. Gut 49, 47–55 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Schamberger, G. P., Phillips, R. L., Jacobs, J. L. & Diez-Gonzalez, F. Reduction of Escherichia coli O157:H7 populations in cattle by addition of colicin E7-producing E. coli to feed. Appl. Environ. Microbiol. 70, 6053–6060 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Smith, J. M., Smith, N. H., O'Rourke, M. & Spratt, B. G. How clonal are bacteria? Proc. Natl Acad. Sci. USA 90, 4384–4388 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Orskov, F. et al. Special Escherichia coli serotypes among enterotoxigenic strains from diarrhoea in adults and children. Med. Microbiol. Immunol. 162, 73–80 (1976).

    Article  CAS  PubMed  Google Scholar 

  32. Milkman, R. Electrophoretic variation in Escherichia coli from natural sources. Science 182, 1024–1026 (1973).

    Article  CAS  PubMed  Google Scholar 

  33. Selander, R. K. & Levin, B. R. Genetic diversity and structure in Escherichia coli populations. Science 210, 545–547 (1980). A seminal work demonstrating the clonal structure of the E. coli population by MLEE analysis.

    Article  CAS  PubMed  Google Scholar 

  34. Miller, R. D. & Hartl, D. L. Biotyping confirms a nearly clonal population structure in Escherichia coli. Evolution 40, 1–12 (1986).

    Article  PubMed  Google Scholar 

  35. Ochman, H. & Selander, R. K. Evidence for clonal population structure in Escherichia coli. Proc. Natl Acad. Sci. USA 81, 198–201 (1984).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Caugant, D. A. et al. Genetic diversity in relation to serotype in Escherichia coli. Infect. Immun. 49, 407–413 (1985).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Desjardins, P., Picard, B., Kaltenbock, B., Elion, J. & Denamur, E. Sex in Escherichia coli does not disrupt the clonal structure of the population: evidence from random amplified polymorphic DNA and restriction-fragment-length polymorphism. J. Mol. Evol. 41, 440–448 (1995).

    Article  CAS  PubMed  Google Scholar 

  38. Milkman, R. & Crawford, I. P. Clustered third-base substitutions among wild strains of Escherichia coli. Science 221, 378–380 (1983).

    Article  CAS  PubMed  Google Scholar 

  39. Ochman, H. & Selander, R. K. Standard reference strains of Escherichia coli from natural populations. J. Bacteriol. 157, 690–693 (1984). The establishment of a reference collection that is representative of E. coli diversity and that has been and is still widely used around the word.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. DuBose, R. F., Dykhuizen, D. E. & Hartl, D. L. Genetic exchange among natural isolates of bacteria: recombination within the phoA gene of Escherichia coli. Proc. Natl Acad. Sci. USA 85, 7036–7040 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Bisercic, M., Feutrier, J. Y. & Reeves, P. R. Nucleotide sequences of the gnd genes from nine natural isolates of Escherichia coli: evidence of intragenic recombination as a contributing factor in the evolution of the polymorphic gnd locus. J. Bacteriol. 173, 3894–3900 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Dykhuizen, D. E. & Green, L. Recombination in Escherichia coli and the definition of biological species. J. Bacteriol. 173, 7257–7268 (1991). A cornerstone paper that demonstrates the presence of recombination in the E. coli species and proposes a definition of the bacterial species that is based on the biological species definition.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Milkman, R. & Bridges, M. M. Molecular evolution of the Escherichia coli chromosome. IV. Sequence comparisons. Genetics 133, 455–468 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Milkman, R. & Stoltzfus, A. Molecular evolution of the Escherichia coli chromosome. II. Clonal segments. Genetics 120, 359–366 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Milkman, R. & Bridges, M. M. Molecular evolution of the Escherichia coli chromosome. III. Clonal frames. Genetics 126, 505–517 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. McKane, M. & Milkman, R. Transduction, restriction and recombination patterns in Escherichia coli. Genetics 139, 35–43 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Milkman, R. et al. Molecular evolution of the Escherichia coli chromosome. V. Recombination patterns among strains of diverse origin. Genetics 153, 539–554 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Guttman, D. S. & Dykhuizen, D. E. Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science 266, 1380–1383 (1994).

    Article  CAS  PubMed  Google Scholar 

  49. Nelson, K., Whittam, T. S. & Selander, R. K. Nucleotide polymorphism and evolution in the glyceraldehyde-3-phosphate dehydrogenase gene (gapA) in natural populations of Salmonella and Escherichia coli. Proc. Natl Acad. Sci. USA 88, 6667–6671 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Hall, B. G. & Sharp, P. M. Molecular population genetics of Escherichia coli: DNA sequence diversity at the celC, crr, and gutB loci of natural isolates. Mol. Biol. Evol. 9, 654–665 (1992).

    CAS  PubMed  Google Scholar 

  51. Milkman, R., Jaeger, E. & McBride, R. D. Molecular evolution of the Escherichia coli chromosome. VI. Two regions of high effective recombination. Genetics 163, 475–483 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Barcus, V. A., Titheradge, A. J. & Murray, N. E. The diversity of alleles at the hsd locus in natural populations of Escherichia coli. Genetics 140, 1187–1197 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Bergthorsson, U. & Ochman, H. Heterogeneity of genome sizes among natural isolates of Escherichia coli. J. Bacteriol. 177, 5784–5789 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Bergthorsson, U. & Ochman, H. Distribution of chromosome length variation in natural isolates of Escherichia coli. Mol. Biol. Evol. 15, 6–16 (1998).

    Article  CAS  PubMed  Google Scholar 

  55. Hendrickson, H. Order and disorder during Escherichia coli divergence. PLoS Genet. 5, e1000335 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Rasko, D. A. et al. The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J. Bacteriol. 190, 6881–6893 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Touchon, M. et al. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 5, e1000344 (2009). A comprehensive paper that uses whole-genome sequences of E. coli to reconcile the occurrence of recombination events and the observed clonal struture of the population, thus allowing phylogenetic analyses to be carried out.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  59. Beaumont, M. A., Zhang, W. & Balding, D. J. Approximate Bayesian computation in population genetics. Genetics 162, 2025–2035 (2002).

    PubMed  PubMed Central  Google Scholar 

  60. Mercier, R. et al. The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 135, 475–485 (2008).

    Article  CAS  PubMed  Google Scholar 

  61. Milkman, R. Recombination and population structure in Escherichia coli. Genetics 146, 745–750 (1997). An insightful perspective by a visionary of the effect of recombination on the E. coli population structure that is still relevant today.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Schubert, S. et al. Role of intraspecies recombination in the spread of pathogenicity islands within the Escherichia coli species. PLoS Pathog. 5, e1000257 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Selander, R. K. et al. Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl. Environ. Microbiol. 51, 873–884 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Goullet, P. & Picard, B. Comparative electrophoretic polymorphism of esterases and other enzymes in Escherichia coli. J. Gen. Microbiol. 135, 135–143 (1989).

    CAS  PubMed  Google Scholar 

  65. Selander, R. K., Caugant, D. A. & Whittam, T. S. in Escherichia coli and Salmonella typhimurium. Cellular and Molecular Biology. (eds Neidhardt, F. C. et al.) 1625–1648 (American Society for Microbiology, Washington, DC, 1987).

  66. Herzer, P. J., Inouye, S., Inouye, M. & Whittam, T. S. Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J. Bacteriol. 172, 6175–6181 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Reid, S. D., Herbelin, C. J., Bumbaugh, A. C., Selander, R. K. & Whittam, T. S. Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406, 64–67 (2000).

    Article  CAS  PubMed  Google Scholar 

  68. Escobar-Paramo, P. et al. Decreasing the effects of horizontal gene transfer on bacterial phylogeny: the Escherichia coli case study. Mol. Phylogenet. Evol. 30, 243–250 (2004).

    Article  CAS  PubMed  Google Scholar 

  69. Wirth, T. et al. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol. Microbiol. 60, 1136–1151 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Johnson, J. R., Owens, K. L., Clabots, C. R., Weissman, S. J. & Cannon, S. B. Phylogenetic relationships among clonal groups of extraintestinal pathogenic Escherichia coli as assessed by multi-locus sequence analysis. Microbes Infect. 8, 1702–1713 (2006).

    Article  CAS  PubMed  Google Scholar 

  71. Gordon, D. M., Clermont, O., Tolley, H. & Denamur, E. Assigning Escherichia coli strains to phylogenetic groups: multi-locus sequence typing versus the PCR triplex method. Environ. Microbiol. 10, 2484–2496 (2008).

    Article  CAS  PubMed  Google Scholar 

  72. Lawrence, J. G., Ochman, H. & Hartl, D. L. Molecular and evolutionary relationships among enteric bacteria. J. Gen. Microbiol. 137, 1911–1921 (1991).

    Article  CAS  PubMed  Google Scholar 

  73. Lecointre, G., Rachdi, L., Darlu, P. & Denamur, E. Escherichia coli molecular phylogeny using the incongruence length difference test. Mol. Biol. Evol. 15, 1685–1695 (1998).

    Article  CAS  PubMed  Google Scholar 

  74. Felsenstein, J. Cases in which parsimony or compatibility methods will be positively misleading. Syst. Zool. 27, 401–410 (1978).

    Article  Google Scholar 

  75. Jaureguy, F. et al. Phylogenetic and genomic diversity of human bacteremic Escherichia coli strains. BMC Genomics 9, 560 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Lescat, M. et al. aes, the gene encoding the esterase B in Escherichia coli, is a powerful phylogenetic marker of the species. BMC Microbiol. 9, 273 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Le Gall, T. et al. Extraintestinal virulence is a coincidental by-product of commensalism in B2 phylogenetic group Escherichia coli strains. Mol. Biol. Evol. 24, 2373–2384 (2007).

    Article  CAS  PubMed  Google Scholar 

  78. Sears, H. J., Brownlee, I. & Uchiyama, J. K. Persistence of individual strains of Escherichia coli in the intestinal tract of man. J. Bacteriol. 59, 293–301 (1950).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Sears, H. J. & Brownlee, I. Further observations on the persistence of individual strains of Escherichia coli in the intestinal tract of man. J. Bacteriol. 63, 47–57 (1952).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Sears, H. J., Janes, H., Saloum, R., Brownlee, I. & Lamoreaux, L. F. Persistence of individual strains of Escherichia coli in man and dog under varying conditions. J. Bacteriol. 71, 370–372 (1956). This and references 78 and 79 are a series of papers published in the 1950s describing the study of many clones from faecal specimens by O tying and introducing the notion of 'resident' and 'transient' strains.

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Bettelheim, K. A., Faiers, M. & Shooter, R. A. Serotypes of Escherichia coli in normal stools. Lancet 2, 1223–1224 (1972).

    CAS  PubMed  Google Scholar 

  82. Caugant, D. A., Levin, B. R. & Selander, R. K. Genetic diversity and temporal variation in the E. coli population of a human host. Genetics 98, 467–490 (1981). The first (and unfortunately unique) paper to have used MLEE to thoroughly study the genetic structure of the commensal E. coli population in a human host over a 1 year period.

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Escobar-Paramo, P. et al. Large-scale population structure of human commensal Escherichia coli isolates. Appl. Environ. Microbiol. 70, 5698–5700 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Skurnik, D. et al. Characteristics of human intestinal Escherichia coli with changing environments. Environ. Microbiol. 10, 2132–2137 (2008). An elegant study using controlled human migration to show the effects of the environment on the E. coli microbiota.

    Article  PubMed  Google Scholar 

  85. Escobar-Paramo, P. et al. Identification of forces shaping the commensal Escherichia coli genetic structure by comparing animal and human isolates. Environ. Microbiol. 8, 1975–1984 (2006).

    Article  CAS  PubMed  Google Scholar 

  86. Caugant, D. A., Levin, B. R. & Selander, R. K. Distribution of multilocus genotypes of Escherichia coli within and between host families. J. Hyg. (Lond.) 92, 377–384 (1984).

    Article  CAS  Google Scholar 

  87. Johnson, J. R., Owens, K., Gajewski, A. & Clabots, C. Escherichia coli colonization patterns among human household members and pets, with attention to acute urinary tract infection. J. Infect. Dis. 197, 218–224 (2008).

    Article  PubMed  Google Scholar 

  88. Cooke, E. M., Hettiaratchy, I. G. & Buck, A. C. Fate of ingested Escherichia coli in normal persons. J. Med. Microbiol. 5, 361–369 (1972).

    Article  CAS  PubMed  Google Scholar 

  89. Poisson, D. M., Borderon, J. C., Amorim-Sena, J. C. & Laugier, J. Evolution of the barrier effects against an exogenous drug-sensitive Escherichia coli strain after single or repeated oral administration to newborns and infants aged up to three months admitted to an intensive-care unit. Biol. Neonate 49, 1–7 (1986).

    Article  CAS  PubMed  Google Scholar 

  90. Myhal, M. L., Laux, D. C. & Cohen, P. S. Relative colonizing abilities of human fecal and K 12 strains of Escherichia coli in the large intestines of streptomycin-treated mice. Eur. J. Clin. Microbiol. 1, 186–192 (1982).

    Article  CAS  PubMed  Google Scholar 

  91. Goullet, P. & Picard, B. Comparative esterase electrophoretic polymorphism of Escherichia coli isolates obtained from animal and human sources. J. Gen. Microbiol. 132, 1843–1851 (1986).

    CAS  PubMed  Google Scholar 

  92. Souza, V., Rocha, M., Valera, A. & Eguiarte, L. E. Genetic structure of natural populations of Escherichia coli in wild hosts on different continents. Appl. Environ. Microbiol. 65, 3373–3385 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Duriez, P. et al. Commensal Escherichia coli isolates are phylogenetically distributed among geographically distinct human populations. Microbiology 147, 1671–1676 (2001).

    Article  CAS  PubMed  Google Scholar 

  94. Zhang, L., Foxman, B. & Marrs, C. Both urinary and rectal Escherichia coli isolates are dominated by strains of phylogenetic group B2. J. Clin. Microbiol. 40, 3951–3955 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  95. Obata-Yasuoka, M., Ba-Thein, W., Tsukamoto, T., Yoshikawa, H. & Hayashi, H. Vaginal Escherichia coli share common virulence factor profiles, serotypes and phylogeny with other extraintestinal E. coli. Microbiology 148, 2745–2752 (2002).

    Article  CAS  PubMed  Google Scholar 

  96. Watt, S. et al. Escherichia coli strains from pregnant women and neonates: intraspecies genetic distribution and prevalence of virulence factors. J. Clin. Microbiol. 41, 1929–1935 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Nowrouzian, F. L., Wold, A. E. & Adlerberth, I. Escherichia coli strains belonging to phylogenetic group B2 have superior capacity to persist in the intestinal microflora of infants. J. Infect. Dis. 191, 1078–1083 (2005).

    Article  CAS  PubMed  Google Scholar 

  98. Gordon, D. M., Stern, S. E. & Collignon, P. J. Influence of the age and sex of human hosts on the distribution of Escherichia coli ECOR groups and virulence traits. Microbiology 151, 15–23 (2005).

    Article  CAS  PubMed  Google Scholar 

  99. Pallecchi, L. et al. Population structure and resistance genes in antibiotic-resistant bacteria from a remote community with minimal antibiotic exposure. Antimicrob. Agents Chemother. 51, 1179–1184 (2007).

    Article  CAS  PubMed  Google Scholar 

  100. Nowrouzian, F. L., Ostblom, A. E., Wold, A. E. & Adlerberth, I. Phylogenetic group B2 Escherichia coli strains from the bowel microbiota of Pakistani infants carry few virulence genes and lack the capacity for long-term persistence. Clin. Microbiol. Infect. 15, 466–472 (2009).

    Article  CAS  PubMed  Google Scholar 

  101. Skurnik, D. et al. Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli. J. Antimicrob. Chemother. 57, 1215–1219 (2006). A clear demonstration of the role of human contact in the emergence of antibiotic resistance in the E. coli microbiota of wild and domesticated animals.

    Article  CAS  PubMed  Google Scholar 

  102. Baldy-Chudzik, K., Mackiewicz, P. & Stosik, M. Phylogenetic background, virulence gene profiles, and genomic diversity in commensal Escherichia coli isolated from ten mammal species living in one zoo. Vet. Microbiol. 131, 173–184 (2008).

    Article  CAS  PubMed  Google Scholar 

  103. Clermont, O. et al. Evidence for a human-specific Escherichia coli clone. Environ. Microbiol. 10, 1000–1006 (2008).

    Article  CAS  PubMed  Google Scholar 

  104. Dixit, S. M. et al. Diversity analysis of commensal porcine Escherichia coli — associations between genotypes and habitat in the porcine gastrointestinal tract. Microbiology 150, 1735–1740 (2004).

    Article  CAS  PubMed  Google Scholar 

  105. Hacker, J. & Kaper, J. B. Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 54, 641–679 (2000).

    Article  CAS  PubMed  Google Scholar 

  106. Levin, B. R. The evolution and maintenance of virulence in microparasites. Emerg. Infect. Dis. 2, 93–102 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Wold, A. E., Caugant, D. A., Lidin-Janson, G., de Man, P. & Svanborg, C. Resident colonic Escherichia coli strains frequently display uropathogenic characteristics. J. Infect. Dis. 165, 46–52 (1992). The first paper to convincingly show that the determinants involved in extraintestinal pathogenicity are associated with long-term persistence in the colon.

    Article  CAS  PubMed  Google Scholar 

  108. Nowrouzian, F. L., Adlerberth, I. & Wold, A. E. Enhanced persistence in the colonic microbiota of Escherichia coli strains belonging to phylogenetic group B2: role of virulence factors and adherence to colonic cells. Microbes Infect. 8, 834–840 (2006).

    Article  CAS  PubMed  Google Scholar 

  109. Moreno, E. et al. Structure and urovirulence characteristics of the fecal Escherichia coli population among healthy women. Microbes Infect. 11, 274–280 (2009).

    Article  PubMed  Google Scholar 

  110. Johnson, J. R., Clabots, C. & Kuskowski, M. A. Multiple-host sharing, long-term persistence, and virulence of Escherichia coli clones from human and animal household members. J. Clin. Microbiol. 46, 4078–4082 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  111. Schierack, P. et al. ExPEC-typical virulence-associated genes correlate with successful colonization by intestinal E. coli in a small piglet group. Environ. Microbiol. 10, 1742–1751 (2008).

    Article  PubMed  Google Scholar 

  112. Sheng, H., Lim, J. Y., Knecht, H. J., Li, J. & Hovde, C. J. Role of Escherichia coli O157:H7 virulence factors in colonization at the bovine terminal rectal mucosa. Infect. Immun. 74, 4685–4693 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Alsam, S. et al. Escherichia coli interactions with Acanthamoeba: a symbiosis with environmental and clinical implications. J. Med. Microbiol. 55, 689–694 (2006).

    Article  PubMed  Google Scholar 

  114. Steinberg, K. M. & Levin, B. R. Grazing protozoa and the evolution of the Escherichia coli O157:H7 Shiga toxin-encoding prophage. Proc. Biol. Sci. 274, 1921–1929 (2007).

    Article  PubMed  Google Scholar 

  115. Diard, M. et al. Caenorhabditis elegans as a simple model to study phenotypic and genetic virulence determinants of extraintestinal pathogenic Escherichia coli. Microbes Infect. 9, 214–223 (2007).

    Article  CAS  PubMed  Google Scholar 

  116. Samie, A. et al. Prevalence and species distribution of E. histolytica and E. dispar in the Venda region, Limpopo, South Africa. Am. J. Trop. Med. Hyg. 75, 565–571 (2006).

    Article  CAS  PubMed  Google Scholar 

  117. Wildschutte, H., Wolfe, D. M., Tamewitz, A. & Lawrence, J. G. Protozoan predation, diversifying selection, and the evolution of antigenic diversity in Salmonella. Proc. Natl Acad. Sci. USA 101, 10644–10649 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Calendar, R. (ed.) The Bacteriophages (Oxford Univ. Press, Oxford, UK, 2006).

    Google Scholar 

  119. Chao, L. & Levin, B. R. Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc. Natl Acad. Sci. USA 78, 6324–6328 (1981).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Kerr, B., Riley, M. A., Feldman, M. W. & Bohannan, B. J. Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature 418, 171–174 (2002).

    Article  CAS  PubMed  Google Scholar 

  121. Andremont, A. Commensal flora may play key role in spreading antibiotic resistance. ASM News 63, 601–607 (2003).

    Google Scholar 

  122. Mazel, D. Integrons: agents of bacterial evolution. Nature Rev. Microbiol. 4, 608–620 (2006).

    Article  CAS  Google Scholar 

  123. Skurnik, D. et al. Integron-associated antibiotic resistance and phylogenetic grouping of Escherichia coli isolates from healthy subjects free of recent antibiotic exposure. Antimicrob. Agents Chemother. 49, 3062–3065 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Mammeri, H., Galleni, M. & Nordmann, P. Role of the Ser-287-Asn replacement in the hydrolysis spectrum extension of AmpC β-lactamases in Escherichia coli. Antimicrob. Agents Chemother. 53, 323–326 (2009).

    Article  CAS  PubMed  Google Scholar 

  125. Deschamps, C. et al. Multiple acquisitions of CTX-M plasmids in the rare D2 genotype of Escherichia coli provide evidence for convergent evolution. Microbiology 155, 1656–1668 (2009).

    Article  CAS  PubMed  Google Scholar 

  126. Picard, B. & Goullet, P. Correlation between electrophoretic types B1 and B2 of carboxylesterase B and sex of patients in Escherichia coli urinary tract infections. Epidemiol. Infect. 103, 97–103 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Johnson, J. R. et al. Association of carboxylesterase B electrophoretic pattern with presence and expression of urovirulence factor determinants and antimicrobial resistance among strains of Escherichia coli that cause urosepsis. Infect. Immun. 59, 2311–2315 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  128. Johnson, J. R. et al. O, K, and H antigens predict virulence factors, carboxylesterase B pattern, antimicrobial resistance, and host compromise among Escherichia coli strains causing urosepsis. J. Infect. Dis. 169, 119–126 (1994).

    Article  CAS  PubMed  Google Scholar 

  129. Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647–1651 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Macpherson, A. J. et al. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288, 2222–2226 (2000).

    Article  CAS  PubMed  Google Scholar 

  131. Kauffmann, F. The serology of the coli group. J. Immunol. 57, 71–100 (1947).

    CAS  PubMed  Google Scholar 

  132. Orskov, F. & Orskov, I. in Methods in Microbiology (ed. Bergan, T.) 43–112 (Academic, London, 1984).

    Google Scholar 

  133. Orskov, F. & Orskov, I. Escherichia coli serotyping and disease in man and animals. Can. J. Microbiol. 38, 699–704 (1992).

    Article  CAS  PubMed  Google Scholar 

  134. Clermont, O., Johnson, J. R., Menard, M. & Denamur, E. Determination of Escherichia coli O types by allele-specific polymerase chain reaction: application to the O types involved in human septicemia. Diagn. Microbiol. Infect. Dis. 57, 129–136 (2007).

    Article  CAS  PubMed  Google Scholar 

  135. Enright, M. C. & Spratt, B. G. Multilocus sequence typing. Trends Microbiol. 7, 482–487 (1999).

    Article  CAS  PubMed  Google Scholar 

  136. Escobar-Paramo, P. et al. A specific genetic background is required for acquisition and expression of virulence factors in Escherichia coli. Mol. Biol. Evol. 21, 1085–1094 (2004).

    Article  CAS  PubMed  Google Scholar 

  137. Clermont, O., Bonacorsi, S. & Bingen, E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 66, 4555–4558 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Mardis, E. R. The impact of next-generation sequencing technology on genetics. Trends Genet. 24, 133–141 (2008).

    Article  CAS  PubMed  Google Scholar 

  139. Liti, G. et al. Population genomics of domestic and wild yeasts. Nature 458, 337–341 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Schacherer, J., Shapiro, J. A., Ruderfer, D. M. & Kruglyak, L. Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458, 342–345 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. MacLean, D., Jones, J. D. & Studholme, D. J. Application of 'next-generation' sequencing technologies to microbial genetics. Nature Rev. Microbiol. 7, 287–296 (2009).

    Google Scholar 

  142. Didelot, X. & Falush, D. Inference of bacterial microevolution using multilocus sequence data. Genetics 175, 1251–1266 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Oshima, K. et al. Complete genome sequence and comparative analysis of the wild-type commensal Escherichia coli strain SE11 isolated from a healthy adult. DNA Res. 15, 375–386 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Iguchi, A. et al. Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain E2348/69. J. Bacteriol. 191, 347–354 (2009).

    Article  CAS  PubMed  Google Scholar 

  145. Walk, S. T. et al. Cryptic lineages of the genus Escherichia. Appl. Environ. Microbiol. 75, 6534–6544 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We are grateful to everyone who has helped us gather our strain collections over the years and continents and to all the members of our laboratory who have analysed these strains, especially P. Escobar-Páramo, T. Le Gall and O. Clermont. E.D. is partially funded by the Fondation pour la Recherche Médicale and O.T. is supported by the Agence Nationale de la Recherche. This review is dedicated to the memory of Thomas S. Whittam, a pioneer in E. coli population genetics, who died on 5 December 2008.

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Authors and Affiliations

  1. INSERM U722 and Université Paris 7 Denis Diderot, Paris, 75018, France

    Olivier Tenaillon, Bertrand Picard & Erick Denamur

  2. Department of Medicine, Harvard Medical School, Channing Laboratory, 181 Longwood Ave, Boston, 02115, Massachusetts, USA

    David Skurnik

  3. Hôpital Avicenne and Université Paris 13 Nord, 93009, Bobigny, France

    Bertrand Picard

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  1. Olivier Tenaillon
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Correspondence to Erick Denamur.

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DATABASES

Entrez Genome Project

Escherichia coli

Escherichia coli K-12

Escherichia fergusonii

Salmonella enterica

FURTHER INFORMATION

Authors' homepage

ECOR collection

MLST database at Michigan State University, USA

MLST database at Institut Pasteur Paris, France

MLST database at University College Cork, Ireland

Glossary

Panmictic

Pertaining to a population in which all individuals are potential recombination partners.

Overdominance

Occurs when natural selection favours the heterozygote over the homozygote in a diploid organism. Selectionists proposed overdominance as the driving force underlying the high level of polymorphism that is observed in natural populations.

Coalescent framework

Coalescent theory is a retrospective model of population genetics. It builds the genealogy of gene copies isolated from a sample of individuals from a population back to a single ancestral copy (known as the most recent common ancestor).

Approximate Bayesian computation

A family of computational likelihood-free inference techniques that operate on summary data (such as population mean or variance) to make broad inferences. They are especially useful in situations in which evaluation of the likelihood is computationally prohibitive or whenever suitable likelihoods are not available.

Linkage disequilibrium

The non-random association of alleles at two or more loci. It describes a situation in which some combinations of alleles or genetic markers occur more or less frequently in a population than would be expected if there were a random association of alleles on the basis of their frequencies.

MLEE-based phenogram

A dendrogram resulting from hierarchical clustering that is computed from multilocus enzyme electrophoresis (MLEE) data.

Long-branch attraction artefact

The erroneous grouping of two or more long branches as sister groups due to methodological artefacts of phylogenetic reconstruction. In the case discussed in this Review, a distant out-group (Salmonella enterica) works as an attractor of long-branched in-group taxa.

Colicin

A protein that is produced by and toxic for some strains of E. coli. Colicins result in the rapid elimination of neighbouring cells that are not resistant to their effects.

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Tenaillon, O., Skurnik, D., Picard, B. et al. The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8, 207–217 (2010). https://doi.org/10.1038/nrmicro2298

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