No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Population Phylogenomics of Extraintestinal Pathogenic

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • PDF
    2.70 MB
  • HTML
    202.12 Kb
  • XML
    189.27 Kb
  • Authors: Jérôme Tourret1,2, Erick Denamur3
  • Editors: Matthew A. Mulvey4, Ann E. Stapleton5, David J. Klumpp6
    Affiliations: 1: Département d’Urologie, Néphrologie et Transplantation Groupe Hospitalier Pitié-Salpêtrière, Assistance Publique-Hôpitaux de Paris, Université Pierre et Marie Curie; 2: UMR 1137 INSERM and Université Paris Diderot, IAME, Sorbonne Paris Cité, 75018 Paris, France; 3: UMR 1137 INSERM and Université Paris Diderot, IAME, Sorbonne Paris Cité, 75018 Paris, France; 4: University of Utah, Salt Lake City, UT; 5: University of Washington, Seattle, WA; 6: Northwestern University, Chicago, IL
  • Source: microbiolspec January 2016 vol. 4 no. 1 doi:10.1128/microbiolspec.UTI-0010-2012
  • Received 09 August 2012 Accepted 23 July 2015 Published 07 January 2016
  • Erick Denamur, [email protected]
image of Population Phylogenomics of Extraintestinal Pathogenic <span class="jp-italic">Escherichia coli</span>
    Preview this microbiology spectrum article:
    Zoom in

    Population Phylogenomics of Extraintestinal Pathogenic , Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/4/1/UTI-0010-2012-1.gif /docserver/preview/fulltext/microbiolspec/4/1/UTI-0010-2012-2.gif
  • Abstract:

    The emergence of genomics over the last 10 years has provided new insights into the evolution and virulence of extraintestinal . By combining population genetics and phylogenetic approaches to analyze whole-genome sequences, it became possible to link genomic features to specific phenotypes, such as the ability to cause urinary tract infections. An chromosome can vary extensively in length, ranging from 4.3 to 6.2 Mb, encoding 4,084 to 6,453 proteins. This huge diversity is structured as a set of less than 2,000 genes (core genome) that are conserved between all the strains and a set of variable genes. Based on the core genome, the history of the species can be reliably reconstructed, revealing the recent emergence of phylogenetic groups A and B1 and the more ancient groups B2, F, and D. Urovirulence is most often observed in B2/F/D group strains and is a multigenic process involving numerous combinations of genes and specific alleles with epistatic interactions, all leading down multiple evolutionary paths. The genes involved mainly code for adhesins, toxins, iron capture systems, and protectins, as well as metabolic pathways and mutation-rate-control systems. However, the barrier between commensal and uropathogenic strains is difficult to draw as the factors that are responsible for virulence have probably also been selected to allow survival of as a commensal in the intestinal tract. Genomic studies have also demonstrated that infections are not the result of a unique and stable isolate, but rather often involve several isolates with variable levels of diversity that dynamically changes over time.

  • Citation: Tourret J, Denamur E. 2016. Population Phylogenomics of Extraintestinal Pathogenic . Microbiol Spectrum 4(1):UTI-0010-2012. doi:10.1128/microbiolspec.UTI-0010-2012.


1. Blattner FR, Plunkett G III, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462. [PubMed][CrossRef]
2. Welch RA, Burland V, Plunkett G III, Redford P, Roesch P, Rasko D, Buckles EL, Liou SR, Boutin A, Hackett J, Stroud D, Mayhew GF, Rose DJ, Zhou S, Schwartz DC, Perna NT, Mobley HL, Donnenberg MS, Blattner FR. 2002. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 99:17020–17024. [PubMed][CrossRef]
3. Perna NT, Plunkett G III, Burland V, Mau B, Glasner JD, Rose DJ, Mayhew GF, Evans PS, Gregor J, Kirkpatrick HA, Pósfai G, Hackett J, Klink S, Boutin A, Shao Y, Miller L, Grotbeck EJ, Davis NW, Lim A, Dimalanta ET, Potamousis KD, Apodaca J, Anantharaman TS, Lin J, Yen G, Schwartz DC, Welch RA, Blattner FR. 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409:529–533. [PubMed][CrossRef]
4. Whitman WB, Coleman DC, Wiebe WJ. 1998. Prokaryotes: The unseen majority. Proc Natl Acad Sci U S A 95:6578–6583. [PubMed][CrossRef]
5. Tenaillon O, Skurnik D, Picard B, Denamur E. 2010. The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8:207–217. [PubMed][CrossRef]
6. Savageau MA. 1983. Escherichia coli habitats, cell types, and molecular mechanisms of gene control. Am Nat 122:732–744. [CrossRef]
7. Russo TA, Johnson JR. 2003. Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect 5:449–456. [PubMed][CrossRef]
8. Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat Rev Microbiol 2:123–140. [PubMed][CrossRef]
9. Russo TA, Johnson JR. 2000. Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J Infect Dis 181:1753–1754. [PubMed][CrossRef]
10. Smith JM, Smith NH, O’Rourke M, Spratt BG. 1993. How clonal are bacteria? Proc Natl Acad Sci U S A 90:4384–4388. [PubMed][CrossRef]
11. Orskov F, Orskov I, Evans DJ Jr, Sack RB, Sack DA, Wadström T. 1976. Special Escherichia coli serotypes among enterotoxigenic strains from diarrhoea in adults and children. Med Microbiol Immunol 162:73–80. [PubMed][CrossRef]
12. Selander RK, Levin BR. 1980. Genetic diversity and structure in Escherichia coli populations. Science 210:545–547. [PubMed][CrossRef]
13. Desjardins P, Picard B, Kaltenböck B, Elion J, Denamur E. 1995. 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. [PubMed][CrossRef]
14. Milkman R, Crawford IP. 1983. Clustered third-base substitutions among wild strains of Escherichia coli. Science 221:378–380. [PubMed][CrossRef]
15. Dykhuizen DE, Green L. 1991. Recombination in Escherichia coli and the definition of biological species. J Bacteriol 173:7257–7268. [PubMed]
16. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P, Bingen E, Bonacorsi S, Bouchier C, Bouvet O, Calteau A, Chiapello H, Clermont O, Cruveiller S, Danchin A, Diard M, Dossat C, Karoui ME, Frapy E, Garry L, Ghigo JM, Gilles AM, Johnson J, Le Bouguénec C, Lescat M, Mangenot S, Martinez-Jéhanne V, Matic I, Nassif X, Oztas S, Petit MA, Pichon C, Rouy Z, Ruf CS, Schneider D, Tourret J, Vacherie B, Vallenet D, Médigue C, Rocha EP, Denamur E. 2009. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5:e1000344. doi:10.1371/journal.pgen.1000344 [CrossRef]
17. Milkman R, Jaeger E, McBride RD. 2003. Molecular evolution of the Escherichia coli chromosome. VI. Two regions of high effective recombination. Genetics 163:475–483. [PubMed]
18. Escobar-Páramo P, Sabbagh A, Darlu P, Pradillon O, Vaury C, Denamur E, Lecointre G. 2004. Decreasing the effects of horizontal gene transfer on bacterial phylogeny: the Escherichia coli case study. Mol Phylogenet Evol 30:243–250. [PubMed][CrossRef]
19. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, Achtman M. 2006. Sex and virulence in Escherichia coli: An evolutionary perspective. Mol Microbiol 60:1136–1151. [PubMed][CrossRef]
20. Walk ST, Alm EW, Gordon DM, Ram JL, Toranzos GA, Tiedje JM, Whittam TS. 2009. Cryptic lineages of the genus Escherichia. Appl Environ Microbiol 75:6534–6544. [PubMed][CrossRef]
21. Clermont O, Gordon DM, Brisse S, Walk ST, Denamur E. 2011. Characterization of the cryptic Escherichia lineages: rapid identification and prevalence. Environ Microbiol 13:2468–2477. [PubMed][CrossRef]
22. Moissenet D, Salauze B, Clermont O, Bingen E, Arlet G, Denamur E, Mérens A, Mitanchez D, Vu-Thien H. 2010. Meningitis caused by Escherichia coli producing TEM-52 extended-spectrum beta-lactamase within an extensive outbreak in a neonatal ward: epidemiological investigation and characterization of the strain. J Clin Microbiol 48:2459–2463. [PubMed][CrossRef]
23. Rasko DA, Rosovitz MJ, Myers GS, Mongodin EF, Fricke WF, Gajer P, Crabtree J, Sebaihia M, Thomson NR, Chaudhuri R, Henderson IR, Sperandio V, Ravel J. 2008. The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 190:6881–6893. [PubMed][CrossRef]
24. Vieira G, Sabarly V, Bourguignon PY, Durot M, Le Fèvre F, Mornico D, Vallenet D, Bouvet O, Denamur E, Schachter V, Médigue C. 2011. Core and panmetabolism in Escherichia coli. J Bacteriol 193:1461–1472. [PubMed][CrossRef]
25. Lukjancenko O, Wassenaar TM, Ussery DW. 2010. Comparison of 61 sequenced Escherichia coli genomes. Microb Ecol 60:708–720. [PubMed][CrossRef]
26. Hacker J, Kaper JB. 2000. Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54:641–679. [PubMed][CrossRef]
27. Hendrickson H. 2009. Order and disorder during Escherichia coli divergence. PLoS Genet 5:e1000335. doi:10.1371/journal.pgen.1000335 [PubMed][CrossRef]
28. Harvey PH, Pagel MD. 1991. The Comparative Method in Evolutionary Biology, Oxford University Press, New York.
29. Rogers BA, Sidjabat HE, Paterson DL. 2011. Escherichia coli O25b-ST131: A pandemic, multiresistant, community-associated strain. J Antimicrob Chemother 66:1–14. [PubMed][CrossRef]
30. Brzuszkiewicz E, Brüggemann H, Liesegang H, Emmerth M, Olschläger T, Nagy G, Albermann K, Wagner C, Buchrieser C, Emody L, Gottschalk G, Hacker J, Dobrindt U. 2006. How to become a uropathogen: comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains. Proc Natl Acad Sci U S A 103:12879–12884. [PubMed][CrossRef]
31. Tourret J, Diard M, Garry L, Matic I, Denamur E. 2010. Effects of single and multiple pathogenicity island deletions on uropathogenic Escherichia coli strain 536 intrinsic extra-intestinal virulence. Int J Med Microbiol 300:435–439. [PubMed][CrossRef]
32. Johnson TJ, Kariyawasam S, Wannemuehler Y, Mangiamele P, Johnson SJ, Doetkott C, Skyberg JA, Lynne AM, Johnson JR, Nolan LK. 2007. The genome sequence of avian pathogenic Escherichia coli strain O1:K1:H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. J Bacteriol 189:3228–3236. [PubMed][CrossRef]
33. Manges AR, Johnson JR, Foxman B, O’Bryan TT, Fullerton KE, Riley LW. 2001. Widespread distribution of urinary tract infections caused by a multidrug-resistant Escherichia coli clonal group. N Engl J Med 345:1007–1013. [PubMed][CrossRef]
34. Lane MC, Mobley HL. 2007. Role of P-fimbrial-mediated adherence in pyelonephritis and persistence of uropathogenic Escherichia coli (UPEC) in the mammalian kidney. Kidney Int 72:19–25. [PubMed][CrossRef]
35. Picard B, Garcia JS, Gouriou S, Duriez P, Brahimi N, Bingen E, Elion J, Denamur E. 1999. The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect Immun 67:546–553. [PubMed]
36. Moriel DG, Bertoldi I, Spagnuolo A, Marchi S, Rosini R, Nesta B, Pastorello I, Corea VA, Torricelli G, Cartocci E, Savino S, Scarselli M, Dobrindt U, Hacker J, Tettelin H, Tallon LJ, Sullivan S, Wieler LH, Ewers C, Pickard D, Dougan G, Fontana MR, Rappuoli R, Pizza M, Serino L. 2010. Identification of protective and broadly conserved vaccine antigens from the genome of extraintestinal pathogenic Escherichia coli. Proc Natl Acad Sci U S A 107:9072–9077. [PubMed][CrossRef]
37. Tenaillon O, Rodríguez-Verdugo A, Gaut RL, McDonald P, Bennett AF, Long AD, Gaut BS. 2012. The molecular diversity of adaptive convergence. Science 335:457–461. [PubMed][CrossRef]
38. Johnson JR, Manges AR, O'Bryan TT, Riley LW. 2002. A disseminated multidrug-resistant clonal group of uropathogenic Escherichia coli in pyelonephritis. Lancet 359:2249–2251. [PubMed][CrossRef]
39. Nicolas-Chanoine MH, Blanco J, Leflon-Guibout V, Demarty R, Alonso MP, Caniça MM, Park YJ, Lavigne JP, Pitout J, Johnson JR. 2008. Intercontinental emergence of Escherichia coli clone O25:H4-ST131 producing CTX-M-15. J Antimicrob Chemother 61:273–281. [PubMed][CrossRef]
40. Peirano G, Schreckenberger PC, Pitout JD. 2011. Characteristics of NDM-1-producing Escherichia coli isolates that belong to the successful and virulent clone ST131. Antimicrob Agents Chemother 55:2986–2988. [PubMed][CrossRef]
41. Johnson JR, Menard ME, Lauderdale TL, Kosmidis C, Gordon D, Collignon P, Maslow JN, Andrasević AT, Kuskowski MA; Trans-Global Initiative for Antimicrobial Resistance Analysis Investigators. 2011. Global distribution and epidemiologic associations of Escherichia coli clonal group A, 1998-2007. Emerg Infect Dis 17:2001–2009. [PubMed][CrossRef]
42. Lescat M, Calteau A, Hoede C, Barbe V, Touchon M, Rocha E, Tenaillon O, Médigue C, Johnson JR, Denamur E. 2009. A module located at a chromosomal integration hot spot is responsible for the multidrug resistance of a reference strain from Escherichia coli clonal group A. Antimicrob Agents Chemother 53:2283–2288. [PubMed][CrossRef]
43. Avasthi TS, Kumar N, Baddam R, Hussain A, Nandanwar N, Jadhav S, Ahmed N. 2011. Genome of multidrug-resistant uropathogenic Escherichia coli strain NA114 from India. J Bacteriol 193:4272–4273. [PubMed][CrossRef]
44. Totsika M, Beatson SA, Sarkar S, Phan MD, Petty NK, Bachmann N, Szubert M, Sidjabat HE, Paterson DL, Upton M, Schembri MA. 2011. Insights into a multidrug resistant Escherichia coli pathogen of the globally disseminated ST131 lineage: genome analysis and virulence mechanisms. PLoS One 6:e26578. doi:10.1371/journal.pone.0026578 [PubMed][CrossRef]
45. Clermont O, Lavollay M, Vimont S, Deschamps C, Forestier C, Branger C, Denamur E, Arlet G. 2008. The CTX-M-15-producing Escherichia coli diffusing clone belongs to a highly virulent B2 phylogenetic subgroup. J Antimicrob Chemother 61:1024–1028. [PubMed][CrossRef]
46. Poirel L, Lagrutta E, Taylor P, Pham J, Nordmann P. 2010. Emergence of metallo-beta-lactamase NDM-1-producing multidrug-resistant Escherichia coli in Australia. Antimicrob Agents Chemother 54:4914–4916. [PubMed][CrossRef]
47. Poirel L, Bonnin RA, Nordmann P. 2011. Analysis of the resistome of a multidrug-resistant NDM-1-producing Escherichia coli strain by high-throughput genome sequencing. Antimicrob Agents Chemother 55:4224–4229. [PubMed][CrossRef]
48. Schubert S, Cuenca S, Fischer D, Heesemann J. 2000. High-pathogenicity island of Yersinia pestis in enterobacteriaceae isolated from blood cultures and urine samples: prevalence and functional expression. J Infect Dis 182:1268–1271. [PubMed][CrossRef]
49. Schubert S, Picard B, Gouriou S, Heesemann J, Denamur E. 2002. Yersinia high-pathogenicity island contributes to virulence in Escherichia coli causing extraintestinal infections. Infect Immun 70:5335–5337. [PubMed][CrossRef]
50. Schubert S, Darlu P, Clermont O, Wieser A, Magistro G, Hoffmann C, Weinert K, Tenaillon O, Matic I, Denamur E. 2009. Role of intraspecies recombination in the spread of pathogenicity islands within the Escherichia coli species. PLoS Pathog 5:e1000257. doi:10.1371/journal.ppat.1000257 [PubMed][CrossRef]
51. Chen SL, Hung CS, Xu J, Reigstad CS, Magrini V, Sabo A, Blasiar D, Bieri T, Meyer RR, Ozersky P, Armstrong JR, Fulton RS, Latreille JP, Spieth J, Hooton TM, Mardis ER, Hultgren SJ, Gordon JI. 2006. Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: A comparative genomics approach. Proc Natl Acad Sci U S A 103:5977–5982. [PubMed][CrossRef]
52. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591. [PubMed][CrossRef]
53. Petersen L, Bollback JP, Dimmic M, Hubisz M, Nielsen R. 2007. Genes under positive selection in Escherichia coli. Genome Res 17:1336–1343. [PubMed][CrossRef]
54. Wiles TJ, Kulesus RR, Mulvey MA. 2008. Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp Mol Pathol 85:11–19. [PubMed][CrossRef]
55. Denamur E, Bonacorsi S, Giraud A, Duriez P, Hilali F, Amorin C, Bingen E, Andremont A, Picard B, Taddei F, Matic I. 2002. High frequency of mutator strains among human uropathogenic Escherichia coli isolates. J Bacteriol 184:605–609. [PubMed][CrossRef]
56. Labat F, Pradillon O, Garry L, Peuchmaur M, Fantin B, Denamur E. 2005. Mutator phenotype confers advantage in Escherichia coli chronic urinary tract infection pathogenesis. FEMS Immunol Med Microbiol 44:317–321. [PubMed][CrossRef]
57. Chattopadhyay S, Dykhuizen DE, Sokurenko EV. 2007. ZPS: visualization of recent adaptive evolution of proteins. BMC Bioinformatics 8:187. [PubMed][CrossRef]
58. Chattopadhyay S, Weissman SJ, Minin VN, Russo TA, Dykhuizen DE, Sokurenko EV. 2009. High frequency of hotspot mutations in core genes of Escherichia coli due to short-term positive selection. Proc Natl Acad Sci U S A 106:12412–12417. [PubMed][CrossRef]
59. Denamur E, Matic I. 2006. Evolution of mutation rates in bacteria. Mol Microbiol 60:820–827. [PubMed][CrossRef]
60. Ansorge WJ. 2009. Next-generation DNA sequencing techniques. N Biotechnol 25:195–203. [PubMed][CrossRef]
61. Clark G, Paszkiewicz K, Hale J, Weston V, Constantinidou C, Penn C, Achtman M, McNally A. 2012. Genomic analysis uncovers a phenotypically diverse but genetically homogeneous Escherichia coli ST131 clone circulating in unrelated urinary tract infections. J Antimicrob Chemother 67:868–877. [PubMed][CrossRef]
62. Lindberg U, Claesson I, Hanson LA, Jodal U. 1978. Asymptomatic bacteriuria in schoolgirls. VIII. Clinical course during a 3-year follow-up. J Pediatr 92:194–199. [PubMed][CrossRef]
63. Sundén F, Håkansson L, Ljunggren E, Wullt B. 2010. Escherichia coli 83972 bacteriuria protects against recurrent lower urinary tract infections in patients with incomplete bladder emptying. J Urol 184:179–185. [PubMed][CrossRef]
64. Zdziarski J, Brzuszkiewicz E, Wullt B, Liesegang H, Biran D, Voigt B, Gronberg-Hernandez J, Ragnarsdottir B, Hecker M, Ron EZ, Daniel R, Gottschalk G, Hacker J, Svanborg C, Dobrindt U. 2010. Host imprints on bacterial genomes--rapid, divergent evolution in individual patients. PLoS Pathog 6:e1001078. doi:10.1371/journal.ppat.1001078 [PubMed][CrossRef]
65. Reeves PR, Liu B, Zhou Z, Li D, Guo D, Ren Y, Clabots C, Lan R, Johnson JR, Wang L. 2011. Rates of mutation and host transmission for an Escherichia coli clone over 3 years. PLoS One 6:e26907. doi:10.1371/journal.pone.0026907 [PubMed][CrossRef]
66. Reid SD, Herbelin CJ, Bumbaugh AC, Selander RK, Whittam TS. 2000. Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406:64–67. [PubMed][CrossRef]
67. Jaureguy F, Landraud L, Passet V, Diancourt L, Frapy E, Guigon G, Carbonnelle E, Lortholary O, Clermont O, Denamur E, Picard B, Nassif X, Brisse S. 2008. Phylogenetic and genomic diversity of human bacteremic Escherichia coli strains. BMC Genomics 9:560. doi:10.1186/1471-2164-9-560 [CrossRef]
68. Clermont O, Bonacorsi S, Bingen E. 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558. [PubMed][CrossRef]
69. Gordon DM, Clermont O, Tolley H, Denamur E. 2008. Assigning Escherichia coli strains to phylogenetic groups: multi-locus sequence typing versus the PCR triplex method. Environ Microbiol 10:2484–2496. [PubMed][CrossRef]
70. Bingen E, Picard B, Brahimi N, Mathy S, Desjardins P, Elion J, Denamur E. 1998. Phylogenetic analysis of Escherichia coli strains causing neonatal meningitis suggests horizontal gene transfer from a predominant pool of highly virulent B2 group strains. J Infect Dis 177:642–650. [PubMed][CrossRef]
71. Bonacorsi S, Clermont O, Houdouin V, Cordevant C, Brahimi N, Marecat A, Tinsley C, Nassif X, Lange M, Bingen E. 2003. Molecular analysis and experimental virulence of French and North American Escherichia coli neonatal meningitis isolates: identification of a new virulent clone. J Infect Dis 187:1895–1906. [PubMed][CrossRef]
72. Rodriguez-Siek KE, Giddings CW, Doetkott C, Johnson TJ, Fakhr MK, Nolan LK. 2005. Comparison of Escherichia coli isolates implicated in human urinary tract infection and avian colibacillosis. Microbiology 151:2097–2110. [PubMed][CrossRef]
73. Moulin-Schouleur M, Répérant M, Laurent S, Brée A, Mignon-Grasteau S, Germon P, Rasschaert D, Schouler C. 2007. Extraintestinal pathogenic Escherichia coli strains of avian and human origin: link between phylogenetic relationships and common virulence patterns. J Clin Microbiol 45:3366–3376. [PubMed][CrossRef]
74. Johnson TJ, Wannemuehler Y, Johnson SJ, Stell AL, Doetkott C, Johnson JR, Kim KS, Spanjaard L, Nolan LK. 2008. Comparison of extraintestinal pathogenic Escherichia coli strains from human and avian sources reveals a mixed subset representing potential zoonotic pathogens. Appl Environ Microbiol 74:7043–7050. [PubMed][CrossRef]
75. Ewers C, Li G, Wilking H, Kiessling S, Alt K, Antáo EM, Laturnus C, Diehl I, Glodde S, Homeier T, Böhnke U, Steinrück H, Philipp HC, Wieler LH. 2007. Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they? Int J Med Microbiol 297:163–176. [PubMed][CrossRef]
76. Zhao L, Gao S, Huan H, Xu X, Zhu X, Yang W, Gao Q, Liu X. 2009. Comparison of virulence factors and expression of specific genes between uropathogenic Escherichia coli and avian pathogenic E. coli in a murine urinary tract infection model and a chicken challenge model. Microbiology 155:1634–1644. [PubMed][CrossRef]
77. Clermont O, Olier M, Hoede C, Diancourt L, Brisse S, Keroudean M, Glodt J, Picard B, Oswald E, Denamur E. 2011. Animal and human pathogenic Escherichia coli strains share common genetic backgrounds. Infect Genet Evol 11:654–662. [PubMed][CrossRef]
78. Johnson TJ, Wannemuehler Y, Kariyawasam S, Johnson JR, Logue CM, Nolan LK. 2012. Prevalence of avian-pathogenic Escherichia coli strain O1 genomic islands among extraintestinal and commensal E. coli isolates. J Bacteriol 194:2846–2853. [PubMed][CrossRef]
79. Mora A, López C, Dabhi G, Blanco M, Blanco JE, Alonso MP, Herrera A, Mamani R, Bonacorsi S, Moulin-Schouleur M, Blanco J. 2009. Extraintestinal pathogenic Escherichia coli O1:K1:H7/NM from human and avian origin: detection of clonal groups B2 ST95 and D ST59 with different host distribution. BMC Microbiol 9:132. doi:10.1186/1471-2180-9-132 [CrossRef]
80. Tivendale KA, Logue CM, Kariyawasam S, Jordan D, Hussein A, Li G, Wannemuehler Y, Nolan LK. 2010. Avian-pathogenic Escherichia coli strains are similar to neonatal meningitis E. coli strains and are able to cause meningitis in the rat model of human disease. Infect Immun 78:3412–3419. [PubMed][CrossRef]
81. Levert M, Zamfir O, Clermont O, Bouvet O, Lespinats S, Hipeaux MC, Branger C, Picard B, Saint-Ruf C, Norel F, Balliau T, Zivy M, Le Nagard H, Cruvellier S, Chane-Woon-Ming B, Nilsson S, Gudelj I, Phan K, Ferenci T, Tenaillon O, Denamur E. 2010. Molecular and evolutionary bases of within-patient genotypic and phenotypic diversity in Escherichia coli extraintestinal infections. PLoS Pathog 6:e1001125. doi:10.1371/journal.ppat.1001125 [PubMed][CrossRef]
82. Bauchart P, Germon P, Brée A, Oswald E, Hacker J, Dobrindt U. 2010. Pathogenomic comparison of human extraintestinal and avian pathogenic Escherichia coli--search for factors involved in host specificity or zoonotic potential. Microb Pathog 49:105–115. [PubMed][CrossRef]
83. Dai J, Wang S, Guerlebeck D, Laturnus C, Guenther S, Shi Z, Lu C, Ewers C. 2010. Suppression subtractive hybridization identifies an autotransporter adhesin gene of E. coli IMT5155 specifically associated with avian pathogenic Escherichia coli (APEC). BMC Microbiol 10:236. doi:10.1136/1471-2180-10-236
84. Yamamoto S, Tsukamoto T, Terai A, Kurazono H, Takeda Y, Yoshida O. 1997. Genetic evidence supporting the fecal-perineal-urethral hypothesis in cystitis caused by Escherichia coli. J Urol 157:1127–1129. [PubMed][CrossRef]
85. Moreno E, Andreu A, Pérez T, Sabaté M, Johnson JR, Prats G. 2006. Relationship between Escherichia coli strains causing urinary tract infection in women and the dominant faecal flora of the same hosts. Epidemiol Infect 134:1015–1023. [PubMed][CrossRef]
86. Jakobsen L, Garneau P, Kurbasic A, Bruant G, Stegger M, Harel J, Jensen KS, Brousseau R, Hammerum AM, Frimodt-Møller N. 2011. Microarray-based detection of extended virulence and antimicrobial resistance gene profiles in phylogroup B2 Escherichia coli of human, meat and animal origin. J Med Microbiol 60:1502–1511. [PubMed][CrossRef]
87. Ramchandani M, Manges AR, DebRoy C, Smith SP, Johnson JR, Riley LW. 2005. Possible animal origin of human-associated, multidrug-resistant, uropathogenic Escherichia coli. Clin Infect Dis 40:251–257. [PubMed][CrossRef]
88. Low DA, Braaten BA, Ling GV, Johnson DL, Ruby AL. 1988. Isolation and comparison of Escherichia coli strains from canine and human patients with urinary tract infections. Infect Immun 56:2601–2609. [PubMed]
89. Johnson JR, Stell AL, Delavari P, Murray AC, Kuskowski M, Gaastra W. 2001. Phylogenetic and pathotypic similarities between Escherichia coli isolates from urinary tract infections in dogs and extraintestinal infections in humans. J Infect Dis 183:897–906. [PubMed][CrossRef]
90. Yuri K, Nakata K, Katae H, Yamamoto S, Hasegawa A. 1998. Distribution of uropathogenic virulence factors among Escherichia coli strains isolated from dogs and cats. J Vet Med Sci 60:287–290. [PubMed][CrossRef]
91. Yuri K, Nakata K, Katae H, Tsukamoto T, Hasegawa A. 1999. Serotypes and virulence factors of Escherichia coli strains isolated from dogs and cats. J Vet Med Sci 61:37–40. [PubMed][CrossRef]
92. Johnson JR, Kaster N, Kuskowski MA, Ling GV. 2003. Identification of urovirulence traits in Escherichia coli by comparison of urinary and rectal E. coli isolates from dogs with urinary tract infection. J Clin Microbiol 41:337–345. [PubMed][CrossRef]
93. Kurazono H, Nakano M, Yamamoto S, Ogawa O, Yuri K, Nakata K, Kimura M, Makino S, Nair GB. 2003. Distribution of the usp gene in uropathogenic Escherichia coli isolated from companion animals and correlation with serotypes and size-variations of the pathogenicity island. Microbiol Immunol 47:797–802. [PubMed][CrossRef]
94. Xia X, Meng J, Zhao S, Bodeis-Jones S, Gaines SA, Ayers SL, McDermott PF. 2011. Identification and antimicrobial resistance of extraintestinal pathogenic Escherichia coli from retail meats. J Food Prot 74:38–44. [PubMed][CrossRef]
95. Tan C, Tang X, Zhang X, Ding Y, Zhao Z, Wu B, Cai X, Liu Z, He Q, Chen H. 2012. Serotypes and virulence genes of extraintestinal pathogenic Escherichia coli isolates from diseased pigs in China. Vet J 192:483–488. [PubMed][CrossRef]
96. Johnson JR, Delavari P, Stell AL, Whittam TS, Carlino U, Russo TA. 2001. Molecular comparison of extraintestinal Escherichia coli isolates of the same electrophoretic lineages from humans and domestic animals. J Infect Dis 183:154–159. [PubMed][CrossRef]
97. Johnson JR, Owens K, Gajewski A, Clabots C. 2008. Escherichia coli colonization patterns among human household members and pets, with attention to acute urinary tract infection. J Infect Dis 197:218–224. [PubMed][CrossRef]
98. Johnson JR, Clabots C. 2006. Sharing of virulent Escherichia coli clones among household members of a woman with acute cystitis. Clin Infect Dis 43:e101–108. [PubMed][CrossRef]
99. Johnson JR, Kuskowski MA, Owens K, Clabots C, Singer RS. 2009. Virulence genotypes and phylogenetic background of fluoroquinolone-resistant and susceptible Escherichia coli urine isolates from dogs with urinary tract infection. Vet Microbiol 136:108–114. [PubMed][CrossRef]
100. Johnson JR, Stell AL. 2000. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J Infect Dis 181:261–272. [PubMed][CrossRef]
101. Jauréguy F, Carbonnelle E, Bonacorsi S, Clec’h C, Casassus P, Bingen E, Picard B, Nassif X, Lortholary O. 2007. Host and bacterial determinants of initial severity and outcome of Escherichia coli sepsis. Clin Microbiol Infect 13:854–862. [PubMed][CrossRef]
102. Vejborg RM, Hancock V, Schembri MA, Klemm P. 2011. Comparative genomics of Escherichia coli strains causing urinary tract infections. Appl Environ Microbiol 77:3268–3278. [PubMed][CrossRef]
103. Guyer DM, Kao JS, Mobley HL. 1998. Genomic analysis of a pathogenicity island in uropathogenic Escherichia coli CFT073: distribution of homologous sequences among isolates from patients with pyelonephritis, cystitis, and catheter-associated bacteriuria and from fecal samples. Infect Immun 66:4411–4417. [PubMed]
104. Parham NJ, Pollard SJ, Chaudhuri RR, Beatson SA, Desvaux M, Russell MA, Ruiz J, Fivian A, Vila J, Henderson IR. 2005. Prevalence of pathogenicity island IICFT073 genes among extraintestinal clinical isolates of Escherichia coli. J Clin Microbiol 43:2425–2434. [PubMed][CrossRef]
105. Johnson JR, O’Bryan TT, Delavari P, Kuskowski M, Stapleton A, Carlino U, Russo TA. 2001. Clonal relationships and extended virulence genotypes among Escherichia coli isolates from women with a first or recurrent episode of cystitis. J Infect Dis 183:1508–1517. [PubMed][CrossRef]
106. Escobar-Páramo P, Clermont O, Blanc-Potard AB, Bui H, Le Bouguénec C, Denamur E. 2004. A specific genetic background is required for acquisition and expression of virulence factors in Escherichia coli. Mol Biol Evol 21:1085–1094. [PubMed][CrossRef]
107. Krieger JN, Dobrindt U, Riley DE, Oswald E. 2011. Acute Escherichia coli prostatitis in previously health young men: bacterial virulence factors, antimicrobial resistance, and clinical outcomes. Urology 77:1420–1425. [PubMed][CrossRef]
108. Kanamaru S, Kurazono H, Nakano M, Terai A, Ogawa O, Yamamoto S. 2006. Subtyping of uropathogenic Escherichia coli according to the pathogenicity island encoding uropathogenic-specific protein: comparison with phylogenetic groups. Int J Urol 13:754–760. [PubMed][CrossRef]
109. Soto SM, Smithson A, Martinez JA, Horcajada JP, Mensa J, Vila J. 2007. Biofilm formation in uropathogenic Escherichia coli strains: relationship with prostatitis, urovirulence factors and antimicrobial resistance. J Urol 177:365–368. [PubMed][CrossRef]
110. Ruiz J, Simon K, Horcajada JP, Velasco M, Barranco M, Roig G, Moreno-Martínez A, Martínez JA, Jiménez de Anta T, Mensa J, Vila J. 2002. Differences in virulence factors among clinical isolates of Escherichia coli causing cystitis and pyelonephritis in women and prostatitis in men. J Clin Microbiol 40:4445–4449. [PubMed][CrossRef]
111. Ghenghesh KS, Elkateb E, Berbash N, Abdel Nada R, Ahmed SF, Rahouma A, Seif-Enasser N, Elkhabroun MA, Belresh T, Klena JD. 2009. Uropathogens from diabetic patients in Libya: virulence factors and phylogenetic groups of Escherichia coli isolates. J Med Microbiol 58:1006–1014. [PubMed][CrossRef]
112. Bert F, Huynh B, Dondero F, Johnson JR, Paugam-Burtz C, Durand F, Belghiti J, Valla D, Moreau R, Nicolas-Chanoine MH. 2011. Molecular epidemiology of Escherichia coli bacteremia in liver transplant recipients. Transpl Infect Dis 13:359–365. [PubMed][CrossRef]
113. Keegan SJ, Graham C, Neal DE, Blum-Oehler G, N’Dow J, Pearson JP, Gally DL. 2003. Characterization of Escherichia coli strains causing urinary tract infections in patients with transposed intestinal segments. J Urol 169:2382–2387. [PubMed][CrossRef]
114. Benton J, Chawla J, Parry S, Stickler D. 1992. Virulence factors in Escherichia coli from urinary tract infections in patients with spinal injuries. J Hosp Infect 22:117–127. [PubMed][CrossRef]
115. Guidoni EB, Dalpra VA, Figueiredo PM, da Silva Leite D, Mimica LM, Yano T, Blanco JE, Toporovski J. 2006. E. coli virulence factors in children with neurogenic bladder associated with bacteriuria. Pediatr Nephrol 21:376–381. [PubMed][CrossRef]
116. Hull RA, Rudy DC, Wieser IE, Donovan WH. 1998. Virulence factors of Escherichia coli isolates from patients with symptomatic and asymptomatic bacteriuria and neuropathic bladders due to spinal cord and brain injuries. J Clin Microbiol 36:115–117. [PubMed]
117. Schlager TA, Whittam TS, Hendley JO, Wilson RA, Bhang J, Grady R, Stapleton A. 2000. Expression of virulence factors among Escherichia coli isolated from the periurethra and urine of children with neurogenic bladder on intermittent catheterization. Pediatr Infect Dis J 19:37–41. [PubMed][CrossRef]
118. Stamm WE. 1991. Catheter-associated urinary tract infections: epidemiology, pathogenesis, and prevention. Am J Med 91:65S–71S. [PubMed][CrossRef]
119. Warren JW, Tenney JH, Hoopes JM, Muncie HL, Anthony WC. 1982. A prospective microbiologic study of bacteriuria in patients with chronic indwelling urethral catheters. J Infect Dis 146:719–723. [PubMed][CrossRef]
120. Schlager TA, Johnson JR, Ouellette LM, Whittam TS. 2008. Escherichia coli colonizing the neurogenic bladder are similar to widespread clones causing disease in patients with normal bladder function. Spinal Cord 46:633–638. [PubMed][CrossRef]
121. Rice JC, Peng T, Kuo YF, Pendyala S, Simmons L, Boughton J, Ishihara K, Nowicki S, Nowicki BJ. 2006. Renal allograft injury is associated with urinary tract infection caused by Escherichia coli bearing adherence factors. Am J Transplant 6:2375–2383. [PubMed][CrossRef]
122. Johnson JR, Johnston B, Clabots C, Kuskowski MA, Pendyala S, Debroy C, Nowicki B, Rice J. 2010. Escherichia coli sequence type ST131 as an emerging fluoroquinolone-resistant uropathogen among renal transplant recipients. Antimicrob Agents Chemother 54:546–550. [PubMed][CrossRef]
123. Wang MC, Tseng CC, Wu AB, Lin WH, Teng CH, Yan JJ, Wu JJ. 2012. Bacterial characteristics and glycemic control in diabetic patients with Escherichia coli urinary tract infection. J Microbiol Immunol Infect 46:24–29. [PubMed][CrossRef]
124. Merçon M, Regua-Mangia AH, Teixeira LM, Irino K, Tuboi SH, Goncalves RT, Santoro-Lopes G. 2010. Urinary tract infections in renal transplant recipients: virulence traits of uropathogenic Escherichia coli. Transplant Proc 42:483–485. [PubMed][CrossRef]
125. Bidet P, Mahjoub-Messai F, Blanco J, Dehem M, Aujard Y, Bingen E, Bonacorsi S. 2007. Combined multilocus sequence typing and O serogrouping distinguishes Escherichia coli subtypes associated with infant urosepsis and/or meningitis. J Infect Dis 196:297–303. [PubMed][CrossRef]
126. Bonacorsi S, Houdouin V, Mariani-Kurkdjian P, Mahjoub-Messai F, Bingen E. 2006. Comparative prevalence of virulence factors in Escherichia coli causing urinary tract infection in male infants with and without bacteremia. J Clin Microbiol 44:1156–1158. [PubMed][CrossRef]
127. Bonacorsi S, Lefèvre S, Clermont O, Houdouin V, Bourrillon A, Loirat C, Aujard Y, Bingen E. 2005. Escherichia coli strains causing urinary tract infection in uncircumcised infants resemble urosepsis-like adult strains. J Urol 173:195–197; discussion 197. [PubMed][CrossRef]
128. Johnson JR, Goullet P, Picard B, Moseley SL, Roberts PL, Stamm WE. 1991. 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. [PubMed]
129. Cereto F, Herranz X, Moreno E, Andreu A, Vergara M, Fontanals D, Roget M, Simó M, González A, Prats G, Genescà J. 2008. Role of host and bacterial virulence factors in Escherichia coli spontaneous bacterial peritonitis. Eur J Gastroenterol Hepatol 20:924–929. [PubMed][CrossRef]
130. Johnson JR, Murray AC, Kuskowski MA, Schubert S, Prère MF, Picard B, Colodner R, Raz R; Trans-Global Initiative for Antimicrobial Resistance Initiative (TIARA) Investigators. 2005. Distribution and characteristics of Escherichia coli clonal group A. Emerg Infect Dis 11:141–145. [PubMed][CrossRef]
131. Skjøt-Rasmussen L, Olsen SS, Jakobsen L, Ejrnaes K, Scheutz F, Lundgren B, Frimodt-Møller N, Hammerum AM. 2012. Escherichia coli clonal group A causing bacteraemia of urinary tract origin. Clin Microbiol Infect 19:656–661. [PubMed][CrossRef]
132. Johnson JR, Porter SB, Zhanel G, Kuskowski MA, Denamur E. 2012. Virulence of Escherichia coli clinical isolates in a murine sepsis model in relation to sequence type ST131 status, fluoroquinolone resistance, and virulence genotype. Infect Immun 80:1554–1562. [PubMed][CrossRef]
133. Johnson JR, Johnston B, Clabots C, Kuskowski MA, Castanheira M. 2010. Escherichia coli sequence type ST131 as the major cause of serious multidrug-resistant E. coli infections in the United States. Clin Infect Dis 51:286–294. [PubMed][CrossRef]
134. Cagnacci S, Gualco L, Debbia E, Schito GC, Marchese A. 2008. European emergence of ciprofloxacin-resistant Escherichia coli clonal groups O25:H4-ST 131 and O15:K52:H1 causing community-acquired uncomplicated cystitis. J Clin Microbiol 46:2605–2612. [PubMed][CrossRef]
135. Williamson DA, Roberts SA, Paterson DL, Sidjabat H, Silvey A, Masters J, Rice M, Freeman JT. 2012. Escherichia coli bloodstream infection after transrectal ultrasound-guided prostate biopsy: implications of fluoroquinolone-resistant sequence type 131 as a major causative pathogen. Clin Infect Dis 54:1406–1412. [PubMed][CrossRef]
136. Gibreel TM, Dodgson AR, Cheesbrough J, Fox AJ, Bolton FJ, Upton M. 2012. Population structure, virulence potential and antibiotic susceptibility of uropathogenic Escherichia coli from Northwest England. J Antimicrob Chemother 67:346–356. [PubMed][CrossRef]
137. Blanco J, Mora A, Mamani R, López C, Blanco M, Dahbi G, Herrera A, Blanco JE, Alonso MP, García-Garrote F, Chaves F, Orellana MÁ, Martínez-Martínez L, Calvo J, Prats G, Larrosa MN, González-López JJ, López-Cerero L, Rodríguez-Baño J, Pascual A. 2011. National survey of Escherichia coli causing extraintestinal infections reveals the spread of drug-resistant clonal groups O25b:H4-B2-ST131, O15:H1-D-ST393 and CGA-D-ST69 with high virulence gene content in Spain. J Antimicrob Chemother 66:2011–2021. [PubMed][CrossRef]
138. Slack E, Hapfelmeier S, Stecher B, Velykoredko Y, Stoel M, Lawson MA, Geuking MB, Beutler B, Tedder TF, Hardt WD, Bercik P, Verdu EF, McCoy KD, Macpherson AJ. 2009. Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism. Science 325:617–620. [PubMed][CrossRef]
139. Nolan LK, Wooley RE, Brown J, Spears KR, Dickerson HW, Dekich M. 1992. Comparison of a complement resistance test, a chicken embryo lethality test, and the chicken lethality test for determining virulence of avian Escherichia coli. Avian Dis 36:395–397. [PubMed][CrossRef]
140. Hung CS, Dodson KW, Hultgren SJ. 2009. A murine model of urinary tract infection. Nat Protoc 4:1230–1243. [PubMed][CrossRef]
141. Smith SN, Hagan EC, Lane MC, Mobley HL. 2010. Dissemination and systemic colonization of uropathogenic Escherichia coli in a murine model of bacteremia. MBio 1. [CrossRef]
142. Johnson JR, Clermont O, Menard M, Kuskowski MA, Picard B, Denamur E. 2006. Experimental mouse lethality of Escherichia coli isolates, in relation to accessory traits, phylogenetic group, and ecological source. J Infect Dis 194:1141–1150. [PubMed][CrossRef]
143. Diard M, Garry L, Selva M, Mosser T, Denamur E, Matic I. 2010. Pathogenicity-associated islands in extraintestinal pathogenic Escherichia coli are fitness elements involved in intestinal colonization. J Bacteriol 192:4885–4893. [PubMed][CrossRef]
144. Landraud L, Jauréguy F, Frapy E, Guigon G, Gouriou S, Carbonnelle E, Clermont O, Denamur E, Picard B, Lemichez E, Brisse S, Nassif X. 2012. Severity of Escherichia coli bacteraemia is independent of the intrinsic virulence of the strains assessed in a mouse model. Clin Microbiol Infect 19:85–90. [PubMed][CrossRef]
145. Lefort A, Panhard X, Clermont O, Woerther PL, Branger C, Mentré F, Fantin B, Wolff M, Denamur E; COLIBAFI Group. 2011. Host factors and portal of entry outweigh bacterial determinants to predict the severity of Escherichia coli bacteremia. J Clin Microbiol 49:777–783. [PubMed][CrossRef]
146. Marschall J, Zhang L, Foxman B, Warren DK, Henderson JP; CDC Prevention Epicenters Program. 2012. Both host and pathogen factors predispose to Escherichia coli urinary-source bacteremia in hospitalized patients. Clin Infect Dis 54:1692–1698. [PubMed][CrossRef]
147. Wendt C, Messer SA, Hollis RJ, Pfaller MA, Herwaldt LA. 1998. Epidemiology of polyclonal gram-negative bacteremia. Diagn Microbiol Infect Dis 32:9–13. [PubMed][CrossRef]
148. Johnson JR, Gajewski A, Lesse AJ, Russo TA. 2003. Extraintestinal pathogenic Escherichia coli as a cause of invasive nonurinary infections. J Clin Microbiol 41:5798–5802. [PubMed][CrossRef]
149. Leflon-Guibout V, Bonacorsi S, Clermont O, Ternat G, Heym B, Nicolas-Chanoine MH. 2002. Pyelonephritis caused by multiple clones of Escherichia coli, susceptible and resistant to co-amoxiclav, after a 45 day course of co-amoxiclav. J Antimicrob Chemother 49:373–377. [PubMed][CrossRef]
150. Tourret J, Aloulou M, Garry L, Tenaillon O, Dion S, Ryffel B, Monteiro RC, Denamur E. 2011. The interaction between a non-pathogenic and a pathogenic strain synergistically enhances extra-intestinal virulence in Escherichia coli. Microbiology 157:774–785. [PubMed][CrossRef]
151. Ferenci T. 2005. Maintaining a healthy SPANC balance through regulatory and mutational adaptation. Mol Microbiol 57:1–8. [PubMed][CrossRef]
152. Hengge-Aronis R. 2002. Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66:373–395. [PubMed][CrossRef]
153. Cooper VS, Schneider D, Blot M, Lenski RE. 2001. Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J Bacteriol 183:2834–2841. [PubMed][CrossRef]
154. Maharjan R, Seeto S, Notley-McRobb L, Ferenci T. 2006. Clonal adaptive radiation in a constant environment. Science 313:514–517. [PubMed][CrossRef]
155. European Committee for Antimicrobial Susceptibility Testing (EUCAST) of the European Society of Clinical Microbiology and Infectious Diseases (ESCMID). 2003. Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by broth dilution. Clin Microbiol Infect 9:ix–xv. [CrossRef]
156. Turnidge JD, Bell JM. 2005. Antimicrobial susceptibility on solid media, p 8–60. In Lorian V (ed), Antibiotics in Laboratory Medicine, 5th ed. Lippincott Williams & Wilkins, Philadelphia.
157. Proctor RA. 2000. Editorial response: coagulase-negative staphylococcal infections: A diagnostic and therapeutic challenge. Clin Infect Dis 31:31–33. [PubMed][CrossRef]
158. Lloyd AL, Henderson TA, Vigil PD, Mobley HL. 2009. Genomic islands of uropathogenic Escherichia coli contribute to virulence. J Bacteriol 191:3469–3481. [PubMed][CrossRef]
159. Lecointre G, Rachdi L, Darlu P, Denamur E. 1998. Escherichia coli molecular phylogeny using the incongruence length difference test. Mol Biol Evol 15:1685–1695. [PubMed][CrossRef]
160. Levin BR. 1996. The evolution and maintenance of virulence in microparasites. Emerg Infect Dis 2:93–102. [PubMed][CrossRef]
161. Le Gall T, Clermont O, Gouriou S, Picard B, Nassif X, Denamur E, Tenaillon O. 2007. Extraintestinal virulence is a coincidental by-product of commensalism in B2 phylogenetic group Escherichia coli strains. Mol Biol Evol 24:2373–2384. [PubMed][CrossRef]
162. Moreno E, Johnson JR, Pérez T, Prats G, Kuskowski MA, Andreu A. 2009. Structure and urovirulence characteristics of the fecal Escherichia coli population among healthy women. Microbes Infect 11:274–280. [PubMed][CrossRef]
163. Ostblom A, Adlerberth I, Wold AE, Nowrouzian FL. 2011. Pathogenicity island markers, virulence determinants malX and usp, and the capacity of Escherichia coli to persist in infants’ commensal microbiotas. Appl Environ Microbiol 77:2303–2308. [PubMed][CrossRef]
164. Moreno E, Andreu A, Pigrau C, Kuskowski MA, Johnson JR, Prats G. 2008. Relationship between Escherichia coli strains causing acute cystitis in women and the fecal E. coli population of the host. J Clin Microbiol 46:2529–2534. [PubMed][CrossRef]
165. Zdziarski J, Svanborg C, Wullt B, Hacker J, Dobrindt U. 2008. Molecular basis of commensalism in the urinary tract: low virulence or virulence attenuation? Infect Immun 76:695–703. [PubMed][CrossRef]
166. Klemm P, Hancock V, Schembri MA. 2007. Mellowing out: adaptation to commensalism by Escherichia coli asymptomatic bacteriuria strain 83972. Infect Immun 75:3688–3695. [PubMed][CrossRef]
167. Le Gall T, Darlu P, Escobar-Páramo P, Picard B, Denamur E. 2005. Selection-driven transcriptome polymorphism in Escherichia coli/Shigella species. Genome Res 15:260–268. [PubMed][CrossRef]
168. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, Balestrino D, Loh E, Gripenland J, Tiensuu T, Vaitkevicius K, Barthelemy M, Vergassola M, Nahori MA, Soubigou G, Régnault B, Coppée JY, Lecuit M, Johansson J, Cossart P. 2009. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459:950–956. [PubMed][CrossRef]
169. Hamburg MA, Collins FS. 2010. The path to personalized medicine. N Engl J Med 363:301–304. [PubMed][CrossRef]
170. Ochman H, Selander RK. 1984. Standard reference strains of Escherichia coli from natural populations. J Bacteriol 157:690–693. [PubMed]

Article metrics loading...



The emergence of genomics over the last 10 years has provided new insights into the evolution and virulence of extraintestinal . By combining population genetics and phylogenetic approaches to analyze whole-genome sequences, it became possible to link genomic features to specific phenotypes, such as the ability to cause urinary tract infections. An chromosome can vary extensively in length, ranging from 4.3 to 6.2 Mb, encoding 4,084 to 6,453 proteins. This huge diversity is structured as a set of less than 2,000 genes (core genome) that are conserved between all the strains and a set of variable genes. Based on the core genome, the history of the species can be reliably reconstructed, revealing the recent emergence of phylogenetic groups A and B1 and the more ancient groups B2, F, and D. Urovirulence is most often observed in B2/F/D group strains and is a multigenic process involving numerous combinations of genes and specific alleles with epistatic interactions, all leading down multiple evolutionary paths. The genes involved mainly code for adhesins, toxins, iron capture systems, and protectins, as well as metabolic pathways and mutation-rate-control systems. However, the barrier between commensal and uropathogenic strains is difficult to draw as the factors that are responsible for virulence have probably also been selected to allow survival of as a commensal in the intestinal tract. Genomic studies have also demonstrated that infections are not the result of a unique and stable isolate, but rather often involve several isolates with variable levels of diversity that dynamically changes over time.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...



Image of FIGURE 1

Click to view


Phylogenetic history, reconstructed from 8 concatenated partial-gene sequences using the Pasteur Institut MLST schema ( 67 ), of 128 strains rooted on . The strains have been chosen to be representative of the species’ genetic diversity and life-styles. They originate from the ECOR collection ( 170 ), our laboratory collection ( 77 ), and from complete genomes available in GenBank. No clade strain is represented, see ( 21 ) for their phylogeny. The strains with a black dot correspond to the strains discussed in the text for which a complete-genome sequence is available. The phylogenetic groups and subgroups (ST complexes) are indicated [see the main text for the correspondence with the ST complexes of ( 19 )]. The EPEC strain E2348/69 belongs to the EPEC-1 group. The arrows indicate 3 famous archetypal strains: the O157:H7 EHEC strain, the laboratory-derived K-12 strain, and the O104:H4 Shiga toxin-producing strain from the 2011 German outbreak, belonging to the E, A, and B1 phylogenetic groups, respectively. This phylogeny is similar to the one obtained from core genomes (data not shown).

Source: microbiolspec January 2016 vol. 4 no. 1 doi:10.1128/microbiolspec.UTI-0010-2012
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Click to view


Analysis of the presence of genes in 20 genomes of ( 16 ). The number of genes present in 1 to 20 (all) genomes is presented. The genes that are present in the 20 genomes represent the core genome (11% of the pan-genome), whereas the genes present in only one strain are strain-specific (51% of the pan-genome). It can be seen that very few genes are between these two extremes. When the genes are categorized according to their origin and functions, it appears that strain-specific genes are mostly from mobile elements and of unknown functions, whereas the core-genome genes are almost exclusively composed of non-mobile genes of known functions. Although some of the strain-specific genes confer adaptive functions as discussed in the text, most of these genes are non-adaptive and thus purged over time ( 16 ).

Source: microbiolspec January 2016 vol. 4 no. 1 doi:10.1128/microbiolspec.UTI-0010-2012
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

Click to view


Schematic representation of two distinct evolutionary scenarios leading to association of a character with virulence. P is for pathogenic (black circle) whereas C stands for commensal (white circle). The character can be the presence of a gene or an allele within a gene. In A, the character has been acquired by chance once in the ancestor of the black strains (red arrow) and is a phylogenetic marker. In B, several independent acquisitions of the character are observed (red arrows), representing a convergence and indicating that this character has been selected and is involved in virulence. The same reasoning can be applied for the loss of a character; in this case the ancestral status is the presence of the character.

Source: microbiolspec January 2016 vol. 4 no. 1 doi:10.1128/microbiolspec.UTI-0010-2012
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4

Click to view


Schematic representation of interactions between bacterial-associated genotypic factors, host-related conditions, and the resulting clinical syndrome. Highly virulent phylogroup B2 strains can be responsible for severe clinical syndromes in patients with no medical conditions, such as pyelonephritis, urosepsis, or prostatitis. They are highly lethal to mice. NB: These strains can also be found as fecal commensals, a situation that can be explained by the “virulence by-product of commensalism” hypothesis. A/B1 phylogenetic-group strains can be responsible for a severe clinical syndrome in debilitated patients. However, they show little lethality in a mouse model measuring intrinsic virulence. In patients with no medical condition, phylogroup A/B1 strains with little virulence potential are usually found in less-severe conditions such as cystitis, asymptomatic bacteriuria, or even in non-pathogenic fecal samples. They do not show any virulence in a mouse model measuring intrinsic virulence. NB: Some B2 strains with reductive evolution inactivating numerous virulence determinants can also cause ABU. These strains are not lethal in the mouse model of septicemia (E. Denamur, personal data). Depending on the virulence-factors/host-condition combination, highly virulent B2 phylogroup strains can also be responsible for a non-severe clinical syndrome, such as cystitis. Such strains show high intrinsic virulence in a mouse model of septicemia. VFs: virulence factors. ABU: asymptomatic bacteriuria. A, B1, B2, D: phylogenetic groups.

Source: microbiolspec January 2016 vol. 4 no. 1 doi:10.1128/microbiolspec.UTI-0010-2012
Permissions and Reprints Request Permissions
Download as Powerpoint

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error