Large-scale genomic sequencing of extraintestinal pathogenic Escherichia coli strains

Genome Research

Volumn 25, Issue 1, 2015, Pages 119-128

  Salipante, Stephen J ^a   Roach, David J ^a   Kitzman, Jacob O ^a   Snyder, Matthew W ^a   Stackhouse, Bethany ^a   Butler Wu, Susan M ^a   Lee, Choli ^a   Cookson, Brad T ^a   Shendure, Jay ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; EXTENDED SPECTRUM BETA LACTAMASE; INVASIN; TRANSPOSASE; VIRULENCE FACTOR; BACTERIAL DNA;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENOME; BACTERIUM ISOLATE; EXTRAINTESTINAL PATHOGENIC ESCHERICHIA COLI; GENE SEQUENCE; GENETIC ASSOCIATION; MOLECULAR EPIDEMIOLOGY; NONHUMAN; PHENOTYPE; PHYLOGENETIC TREE; PRIORITY JOURNAL; ADOLESCENT; ADULT; AGED; CHILD; CLASSIFICATION; DNA SEQUENCE; ESCHERICHIA COLI; FEMALE; GENE LIBRARY; GENETICS; HUMAN; INFANT; ISOLATION AND PURIFICATION; LONGITUDINAL STUDY; MALE; MICROBIOLOGY; MIDDLE AGED; MULTIDRUG RESISTANCE; NEWBORN; PHYLOGENY; PRESCHOOL CHILD; PROCEDURES; STATISTICAL MODEL; URINARY TRACT INFECTION; VERY ELDERLY; YOUNG ADULT;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; CHILD; CHILD, PRESCHOOL; DNA, BACTERIAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; FEMALE; GENE LIBRARY; GENETIC ASSOCIATION STUDIES; GENOME, BACTERIAL; HUMANS; INFANT; INFANT, NEWBORN; LOGISTIC MODELS; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; PHENOTYPE; PHYLOGENY; SEQUENCE ANALYSIS, DNA; URINARY TRACT INFECTIONS; VIRULENCE FACTORS; YOUNG ADULT;

EID: 84920650884     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.180190.114     Document Type: Article

References (76)

1. Adams-Sapper S, Diep BA, Perdreau-Remington F, Riley LW. 2013. Clonal composition and co mmunity clustering of drug-susceptible and-resistant Escherichia coli isolates from bloodstream infections. Antimicrob Agents Chemother 57: 490-497.
2. Alam MT, Petit RA III, Crispell EK, Thornton TA, Conneely KN, Jiang Y, Satola SW, Read TD. 2014. Dissecting vancomycin-intermediate resistance in Staphylococcus aureus using genome-wide association. Genome Biol Evol 6: 1174-1185.
3. Alsterlund R, Axelsson C, Olsso n-Liljequist B. 2012. Long-term carriage of extended-spectrum b-lactamase-producing Escherichia coli. Scand J Infect Dis 44: 51-54.
4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215: 403-410.
5. Barrick JE Yu DS Yoon SH Jeong H Oh TK Schneider D Lenski RE Kim JF. 2009 Genome evolution and adaptation in a long-term experiment with Escherichia coli Nature 461 1243-1247.
6. Buckles EL, Bahrani-Mougeot FK, Molina A, Lockatell CV, Johnson DE, Drachenberg CB, Burland V, Blattner FR, Donnenberg MS. 2004. Identification and characterization of a novel uropathogenic Escherichia coli-associated fimbrial gene cluster. Infect Immun 72: 3890-3901.
7. Carlos C, Pires MM, Stoppe NC, Hachich EM, Sato MI, Gomes TA, Amaral LA, Ottoboni LM. 2010. Escherichia coli phylogenetic group determination and its application in the identification of the major animal source of fecal contamination. BMC Microbiol 10: 161.
8. Chen L, Xiong Z, Sun L, Yang J, Jin Q. 2012. VFDB 2012 update: Toward the genetic diversity and molecular evolution of bacterial virulence factors. Nucleic Acids Res 40: D641-D645.
9. Chin CS, Sorenso n J, Harris JB, Robins WP, Charles RC, Jean-Charles RR, Bullard J,Webster DR, Kasarskis A, Peluso P, et al. 2011. The origin of the Haitian cholera outbreak strain. N Engl J Med 364: 33-42.
10. Clermont O, Bonacorsi S, Bingen E. 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66: 4555-4558.
11. Colpan A, Johnston B, Porter S, Clabots C, Anway R, Thao L, Kuskowski MA, Tchesnokova V, Sokurenko EV, Johnson JR, et al. 2013. Escherichia coli sequence type 131 (ST131) subclone H30 as an emergent multidrugresistant pathogen among US veterans. Cl in Infect Dis 57: 1256-1265.
12. Delcher AL, Bratke KA, Powers EC, Salzberg SL. 2007. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23: 673-679.
13. De lsuc F, Brinkmann H, Philippe H. 2005. Phylogenomics and the reconstruction of the tree of life. Nat Rev Genet 6: 361-375.
14. Denich K, Blyn LB, Craiu A, Braaten BA, Hardy J, Low DA, O' Hanley PD. 1991. DNA sequences of three papA genes from uropathogenic Escherichia coli strains: Evidence of structural and serological conservation. Infect Immun 59: 3849-3858.
15. Didelot X, Bowden R, Wilson D J, Peto TE, Crook DW. 2012. Transforming clinical microbiology with bacterial genome sequencing. Nat Rev Genet 13: 601-612.
16. Escobar-Paramo P, Le Menac'h A, Le Gall T, Amorin C, Gouriou S, Picard B, Skurnik D, Denamur E. 2006. Identification of forces shaping the commensal Escherichia coli genetic structure by comparing animal and human isolates. Environ Microbiol 8: 1975-1984.
17. Falush D, Bowden R. 2006. Genom e-wide association mapping in bacteria? Trends Microbiol 14: 353-355.
18. FarhatMR, Shapiro BJ, Kieser KJ, Sultana R, Jacobson KR, Victor TC,Warren RM, Streicher EM, Calver A, Sloutsky A, et al. 2013. Genomic analysis identifies targets of convergent positive selection in drug-resistant Mycobacterium tuberculosis. Nat Genet 45: 1183-1189.
19. Foxman B, Zhang L, Tallman P, Andree BC, Geiger AM, Koopm an JS, Gillespie BW, Palin KA, Sobel JD, Rode CK, et al. 1997. Transmission of uropathogens between sex partners. J Infect Dis 175: 989-992.
20. Gibreel TM, Dodgson AR, Cheesbrough J, Fo x 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.
21. Gupta SK, Nanda V, Malviya P, Jacobs N, Naheed Z, Joseph T. 2013. An unusual case of early onset persistent Escherichia coli septicemia associated with endocarditis. AJP reports 3: 105-106.
22. Hall BG, Cardena s H, Barlow M. 2013. Using complete genome comparisons to identify sequences whose presence accurately predicts clinically important phenotypes. PLoS ONE 8: E68901.
23. Hashimoto M, Ichimura T, Mizoguchi H, Tanaka K, Fujimitsu K, Keyamura K, Ote T, Yamakawa T, Yamazaki Y, Mori H, et al. 2005. Cell size and nucleoid organization of engineered Escherichia coli cells with a reduced genome. Mol Microbiol 55: 137-149.
24. Hilty M, Betsch BY, Bogli-Stuber K, Heiniger N, Stadler M, Kuffer M, Kronenberg A, Rohrer C, Aebi S, Endimiani A, et al. 2012. Transmission dynamics of extended-spectrum b-lactamase-producing Enter obacteriaceae in the tertiary care hospital and the household setting. Clin Infect Dis 55: 967-975.
25. Huang DW Sherman BT Lempicki RA. 2009 Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 4 44-57.
26. Jaureguy F, Landraud L, Passet V, Diancourt L, Frapy E, Guigon G, Carbonnelle E, Lortholary O, Clermont O, Denamur E, et al. 2008. Phylogenetic and genomic diversity of human bacteremic Escherichia coli strains. BMC Genomics 9: 560.
27. Johnson JR, Goullet P, Picard B, Moseley SL, Roberts PL, Stamm WE. 1991. Association of ca rboxylesterase 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.
28. John son JR, Stell AL, Scheutz F, O'Bryan TT, Russo TA, Carlino UB, Fasching C, Kavle J, Van Dijk L, Gaastra W. 2000. Analysis of the F antigen-specific papA alleles of extraintestinal pathogenic Escherichia coli us ing a novel multiplex PCR-based assay. Infect Immun 68: 1587-1599.
29. Johnson JR, Owens KL, Clabots CR, Weissman SJ, Cannon SB. 2006. Phylogenetic relationships among clonal groups of extraintestinal pa thogenic Escherichia coli as assessed by multi-locus sequence analysis. Microbes Infect 8: 1702-1713.
30. 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.
31. Kaas RS, Friis C, Ussery DW, Aarestrup FM. 2012. Estimating variation within the genes and infer ring the phylogeny of 186 sequenced diverse Escherichia coli genomes. BMC Genomics 13: 577.
32. Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat Rev Microbiol 2: 123-140.
33. Kennedy AD, Porcella SF, Martens C, Whitney AR, Braughton KR, Chen L, Craig CT, Tenover FC, Kreiswirth BN, Musser JM, et al. 2010. Complete nucleotide sequence analysis of plasmids in strains of Staph ylococcus aureus clone USA300 reveals a high level of identity among isolates with closely related core genome sequences. J Clin Microbiol 48: 4504-4511.
34. Koser CU, Holden MT, Ellington MJ, Cartwright EJ, Brown NM, Ogilvy-Stuart AL, Hsu LY, Chewapreecha C, Croucher NJ, Harris SR, et al. 2012. Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med 366: 2267-2275.
35. Kumar S, Filipski AJ, Battistuzzi FU, Kosakovsky Pond SL, Tamura K. 2012. Statistics and truth in phylogenomics. Mol Biol Evol 29: 457-472.
36. Laabei M, Recker M, Rudkin JK, Alde ljawi M, Gulay Z, Sloan TJ, Williams P, Endres JL, Bayles KW, Fey PD, et al. 2014. Predicting the virulence of MRSA from its genome sequence. Genome Res 24: 839-849.
37. Lau SH, Reddy S, Cheesbrough J, Bolton FJ, Willshaw G, Cheasty T, Fox AJ, Upton M. 2008. Major uropathogenic Escherichia coli strain isolated in the northwest of England identified by multilocus sequence typing . J Clin Microbiol 46: 1076-1080.
38. 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.
39. Lee H, Popodi E, Tang H, Foster PL. 2012. Rate and molecular spectrum of spontaneous mutations in the bacterium Escherichia coli as determined by whole-genome sequencing. Proc Natl Acad Sci 109: E2774-E2783.
40. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
41. Li W, Godzik A. 2006. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.
42. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
43. Lieberman TD, Michel JB, Aingaran M, Potter-Bynoe G, Roux D, DavisMRJr, Skurnik D, Leiby N, Lipuma JJ, Goldberg JB, et al. 2011. Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Genet 43: 1275-1280.
44. Lindberg F, Lund B, Johansson L, Normark S. 1987. Localization of the receptor-binding protein adhesin at the tip of the bacterial pilus. Nature 328: 84-87.
45. Lindsay JA. 2014. Evolution of Staphylococcus aureus and MRSA during outbreaks. Infect Genet Evol 21: 548-553.
46. Luo C Walk ST Gordon DM Feldgarden M Tiedje JM Konstantinidis KT 2011 Genome sequencing of environmental Escherichia coli expan ds understanding of the ecology and speciation of the model bacterial species. Proc Natl Acad Sci 108 7200-7205.
47. Manges AR, Dietrich PS, Riley LW. 2004. Multidrug-resistant Escherichia coli clonal groups causing community-acquired pyelonephritis. Clin Infect Dis 38: 329-334
48. Manges AR, Tabor H, Tellis P, Vincent C, Tellier PP. 2008. Endemic and epidemic lineages of Escherichia coli that cause urinary tract infections. Emerg Infect Dis 14: 1575 -1583.
49. Martin GS, Mannino DM, Eaton S, Moss M. 2003. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 348: 1546-1554.
50. Miller RM, Price JR, Batty EM, Didelot X, Wyllie D, Golubchik T, Crook DW, Paul J, Peto TE,Wilson DJ, et al. 2014. Healthcare-associated outbreak of meticillin-resistant Staphylococcus aureus b acteraemia: Role of a cryptic variant of an epidemic clone. J Hosp Infect 86: 83-89.
51. Morgan-Linnell SK, Becnel Boyd L, Steffen D, Zechiedrich L. 2009. Mechanisms accounting for fluoroquinolone resistance in Escherichia coli clinical isolates. Antimicrob Agents Chemother 53: 235-241.
52. Nowrouzian FL, Adlerberth I, Wold AE. 2006. 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.
53. 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.
54. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D. 2006. Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38: 904-909.
55. Price MN, Dehal PS, Arkin AP. 2010. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5: E9490.
56. Price LB, Johnson JR, Aziz M, Clabots C, Johnston B, Tchesnokova V, Nordstrom L, Billig M, Chattopadhyay S, Stegger M, et al. 2013. The epidemic of extended-spectrum-b-lactamase-producing Escherichia coli ST131 is driven by a singl e highly pathogenic subclone, H30-Rx. mBio 4: E00377-e00313.
57. R Core Team. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
58. Ramos NL, Saayman ML, Chapman TA, Tucker JR, Smith HV, Faoagali J, Chin JC, Brauner A, Katouli M. 2010. Genetic relatedness and virulence gene profiles of Escherichia coli strains isolated from septicaemic and uroseptic patients. Eur J Clin Microbiol Infect Dis 29: 15-23.
59. RaskoDA, Rosovitz MJ,Myers GS,Mongodin EF, FrickeWF, Gajer P, Crabtree J, Sebaihia M, Thomson NR, Chaudhuri R, et al. 2008. The pangenome structure of Escherichia coli: Comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 190: 6881-6893.
60. Ron EZ. 2010 Distribution and evolution of virulence factors in septicemic Escherichia coli. Int J Med Microbiol 300: 367-370.
61. Samet A, Sledzinska A, Krawczyk B,Hellmann A, Nowicki S, Kur J, Nowicki B. 2013. Leukemia and risk of recurrent Escherichia coli bacteremia: Genotyping implicates E. coli translocation from the colon to the bloodstream. Eur J Clin Microbiol Infect Dis 32: 1393-1400.
62. Sanjar F, Hazen TH, Shah SM, Koenig SS, Agrawal S, Daugherty S, Sadzewicz L, Tallon LJ, Ma mmel MK, Feng P, et al. 2014. Genome sequence of Escherichia coli O157:H7 strain 2886-75, associated with the first reported case of human infection in the United States. Genome Announc 2: E01120.
63. Sannes MR, Kuskowski MA, Owens K, Gajewski A, Johnson JR. 2004. Virulence factor profiles and phylogenetic background of Escherichia coli isolates from veteranswith bacteremia and uninfected control subjects. J Infect Dis 190: 2121-2128.
64. Schatz MC, Phillippy AM. 2012. The rise of a digital immune system. GigaScience 1: 4.
65. SenGupta DJ, Cummings LA, Hoogestraat DR, Butler-Wu SM, Shendure J, Cookson BT, Salipante SJ. 2014. Whole-genome sequencing for highresolution investigation of methicillin-resistant Staphylococcus aureus epidemiology and genome plasticity. J Clin Microbiol 52: 2787-2796.
66. Sheppard SK, Didelot X,Meric G, Torralbo A, Jolley KA, Kelly DJ, Bentley SD, Maiden MC, Parkhill J, Falush D. 2013. Genome-wide as sociation study identifies vitamin B5 biosynthesis as a host specificity factor in Campylobacter. Proc Natl Acad Sci 110: 11923-11927.
67. Simpson JT Wong K Jackman SD Schein JE Jones SJ Birol I. 2009. ABySS: A parallel assembler for short read sequence data. Genome Res. 19. 1117-1123.
68. Snitkin ES, Zelazny AM, Thomas PJ, Stock F, Henderson DK, Palmore TN, Segre JA. 2012. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med 4: 148ra116.
69. Spurbeck RR, Dinh PC Jr,Walk ST, Stapleton AE, Hooton TM, Nolan LK, Kim KS, Johnson JR, Mobley HL. 2012. Escherichia coli isolates that carry vat, fyuA, chuA, and yfcV efficiently colonize the urinary tract. Infect Immun 80: 4115-4122.
70. Tartof SY, Solberg OD, Manges AR, Riley LW. 2005. Analysis of a uropathogenic Escherichia coli clonal group by multilocus sequence typing. J Clin Microbiol 43: 5860-5864.
71. Telli M, Guiral E, Martinez JA, Almela M, Bosch J, Vila J, Soto SM. 2010. Pre valence of enterotoxins among Escherichia coli isolates causing bacteraemia. FEMS Microbiol Lett 306: 117-121.
72. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtre e J, Jones AL, Durkin AS, et al. 2005. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: Implications for the microbial " pan-genome". Proc Natl Acad Sci 102: 13950-13955.
73. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P, Bingen E, Bonacorsi S, Bouchier C, Bouvet O, et al. 2009. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5: E1000344.
74. Toval F, Kohler CD, Vogel U,Wagenlehner F, Mellmann A, Fruth A, Schmidt MA, Karch H, Bielaszewska M, Dobrindt U. 2014. Characterization of Escherichia coli isolates from hospital inpatients or outpatients with urinary tract infection. J Clin Microbiol 52: 407-418.
75. Walker TM, Ip CL, Harrell RH, Evans JT, Kapatai G, Dedicoat MJ, Eyre DW, Wilson DJ, Hawkey PM, Crook DW, et al. 2013. Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: A retrospective observational study. Lancet Infect Dis 13: 137-146.
76. Zhou Y, L iang Y, Lynch KH, Dennis JJ,Wishart DS. 2011. PHAST: A fast phage search tool. Nucleic Acids Res 39: W347-352.