Systematic longitudinal survey of invasive Escherichia coli in England demonstrates a stable population structure only transiently disturbed by the emergence of ST131

Genome Research

Volumn 27, Issue 8, 2017, Pages 1437-1449

  Kallonen, Teemu ^a   Brodrick, Hayley J ^b   Harris, Simon R ^a   Corander, Jukka ^a,c,d   Brown, Nicholas M ^e,f   Martin, Veronique ^g   Peacock, Sharon J ^a,b,f,h   Parkhill, Julian ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF OSLO   (Norway)

^e ADDENBROOKE S HOSPITAL   (United Kingdom)

^f CAMBRIDGE UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^g 11 the Wharf   (United Kingdom)

^h LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMIKACIN; AMOXICILLIN; AMOXICILLIN PLUS CLAVULANIC ACID; AMPICILLIN; ANTIBIOTIC AGENT; AZTREONAM; BETA LACTAM ANTIBIOTIC; CEFALOTIN; CEFEPIME; CEFOTAXIME; CEFTAZIDIME; CEFUROXIME; CEFUROXIME AXETIL; CIPROFLOXACIN; ERTAPENEM; GENTAMICIN; IMIPENEM; MEROPENEM; TIGECYCLINE; TOBRAMYCIN; TRIMETHOPRIM; VIRULENCE FACTOR; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTEREMIA; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ISOLATE; COMMENSAL; ENGLAND; ESCHERICHIA COLI; ESCHERICHIA COLI ST131; ESPC GENE; FREQUENCY DEPENDENT SELECTION; HUMAN; LONGITUDINAL STUDY; MULTIDRUG RESISTANCE; NONHUMAN; PHYLOGENY; POPULATION DYNAMICS; POPULATION STRUCTURE; PREVALENCE; PRIORITY JOURNAL; RETROSPECTIVE STUDY; WHOLE GENOME SEQUENCING; EPIDEMIOLOGY; ESCHERICHIA COLI INFECTION; GENETICS; MICROBIOLOGY; PATHOGENICITY;

ANTI-BACTERIAL AGENTS; BACTEREMIA; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ENGLAND; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; HUMANS; LONGITUDINAL STUDIES; PHYLOGENY;

EID: 85026656976     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.216606.116     Document Type: Article

References (77)

1. Adams-Sapper S, Diep BA, Perdreau-Remington F, Riley LW. 2013. Clonal composition and community clustering of drug-susceptible and-resistant Escherichia coli isolates from bloodstream infections. Antimicrob Agents Chemother 57: 490-497.
2. Alhashash F, Weston V, Diggle M, McNally A. 2013. Multidrug-resistant Escherichia coli bacteremia. Emerg Infect Dis 19: 1699-1701.
3. Alhashash F, Wang X, Paszkiewicz K, Diggle M, Zong Z, McNally A. 2016. Increase in bacteraemia cases in the East Midlands region of the UK due to MDR Escherichia coli ST73: high levels of genomic and plasmid diversity in causative isolates. J Antimicrob Chemother 71: 339-343.
4. Allsopp LP, Totsika M, Tree JJ, Ulett GC, Mabbett AN, Wells TJ, Kobe B, Beatson SA, Schembri MA. 2010. UpaH is a newly identified autotransporter protein that contributes to biofilm formation and bladder colonization by uropathogenic Escherichia coli CFT073. Infect Immun 78: 1659-1669.
5. Allsopp LP, Beloin C, Moriel DG, Totsika M, Ghigo JM, Schembri MA. 2012. Functional heterogeneity of the UpaH autotransporter protein from uropathogenic Escherichia coli. J Bacteriol 194: 5769-5782.
6. Andrews JM. 2001. Determination of minimum inhibitory concentrations. J Antimicrob Chemother 48(Suppl 1): 5-16.
7. Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV. 2012. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol 29: 2157-2167.
8. Baele G, Li WL, Drummond AJ, Suchard MA, Lemey P. 2013. Accurate model selection of relaxed molecular clocks in Bayesian phylogenetics. Mol Biol Evol 30: 239-243.
9. Banerjee R, Johnston B, Lohse C, Chattopadhyay S, Tchesnokova V, Sokurenko EV, Johnson JR. 2013. The clonal distribution and diversity of extraintestinal Escherichia coli isolates vary according to patient characteristics. Antimicrob Agents Chemother 57: 5912-5917.
10. Ben Zakour NL, Alsheikh-Hussain AS, Ashcroft MM, Khanh Nhu NT, Roberts LW, Stanton-Cook M, Schembri MA, Beatson SA. 2016. Sequential acquisition of virulence and fluoroquinolone resistance has shaped the evolution of Escherichia coli ST131. MBio 7: e00347-16.
11. Boetzer M, Pirovano W. 2012. Toward almost closed genomes with GapFiller. Genome Biol 13: R56.
12. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. 2011. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27: 578-579.
13. Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ. 2005. Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63: 219-228.
14. Chatzidaki-Livanis M, Geva-Zatorsky N, Comstock LE. 2016. Bacteroides fragilis type VI secretion systems use novel effector and immunity proteins to antagonize human gut Bacteroidales species. Proc Natl Acad Sci 113: 3627-3632.
15. Chen SL, Hung CS, Xu J, Reigstad CS, Magrini V, Sabo A, Blasiar D, Bieri T, Meyer RR, Ozersky P, et al. 2006. Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. Proc Natl Acad Sci 103: 5977-5982.
16. Chen L, Hu H, Chavda KD, Zhao S, Liu R, Liang H, Zhang W,Wang X, Jacobs MR, Bonomo RA, et al. 2014. Complete sequence of a KPC-producing IncN multidrug-resistant plasmid from an epidemic Escherichia coli sequence type 131 strain in China. Antimicrob Agents Chemother 58: 2422-2425.
17. Cheng L, Connor TR, Siren J, Aanensen DM, Corander J. 2013. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol Biol Evol 30: 1224-1228.
18. 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.
19. Clermont O, Bonacorsi S, Bingen E. 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66: 4555-4558.
20. Clermont O, Christenson JK, Denamur E, Gordon DM. 2013. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 5: 58-65.
21. Corander J, Marttinen P, Siren J, Tang J. 2008. Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9: 539.
22. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA, Bentley SD, Parkhill J, Harris SR. 2015. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 43: e15.
23. Day MJ, Doumith M, Abernethy J, Hope R, Reynolds R, Wain J, Livermore DM, Woodford N. 2016. Population structure of Escherichia coli causing bacteraemia in the UK and Ireland between 2001 and 2010. J Antimicrob Chemother 71: 2139-2142.
24. de Kraker ME, Jarlier V, Monen JC, Heuer OE, van de Sande N, Grundmann H. 2013. The changing epidemiology of bacteraemias in Europe: trends from the European Antimicrobial Resistance Surveillance System. Clin Microbiol Infect 19: 860-868.
25. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214.
26. Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29: 1969-1973.
27. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
28. Elixhauser A, Friedman B, Stranges E. 2011. Septicemia in U.S. Hospitals, 2009: statistical brief #122. Agency for Healthcare Research and Quality, Rockville, MD.
29. ESPAUR. 2015. English surveillance programme for antimicrobial utilisation and resistance (ESPAUR) 2010 to 2014: report 2015. Public Health England, London.
30. Fitch WM. 1971. Toward defining course of evolution: minimum change for a specific tree topology. Syst Zool 20: 406-416.
31. Forde BM, Ben Zakour NL, Stanton-Cook M, Phan MD, Totsika M, Peters KM, Chan KG, SchembriMA, Upton M, Beatson SA. 2014. The complete genome sequence of Escherichia coli EC958: a high quality reference sequence for the globally disseminated multidrug resistant E. coli O25b: H4-ST131 clone. PLoS One 9: e104400.
32. Gerver R, Mihalkova M, Abernethy J, Bou-Antoun S, Nsonwu O, Kausar S, Wasti S, Apraku D, Davies J, Hope R. 2015. Annual epidemiological commentary: mandatory MRSA, MSSA and E. coli bacteraemia and C. difficile infection data, 2014/15, p. 81. Public Health England, London.
33. 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.
34. Guyer DM, Henderson IR, Nataro JP, Mobley HL. 2000. Identification of Sat, an autotransporter toxin produced by uropathogenic Escherichia coli. Mol Microbiol 38: 53-66.
35. Hazen TH, Donnenberg MS, Panchalingam S, Antonio M, Hossain A, Mandomando I, Ochieng JB, Ramamurthy T, Tamboura B, Qureshi S, et al. 2016. Genomic diversity of EPEC associated with clinical presentations of differing severity. Nat Microbiol 1: 15014.
36. Horner C, Fawley W, Morris K, Parnell P, Denton M, Wilcox M. 2014. Escherichia coli bacteraemia: 2 years of prospective regional surveillance (2010-12). J Antimicrob Chemother 69: 91-100.
37. Ingle D, Valcanis M, Kuzevski A, Tauschek M, Inouye M, Stinear T, Levine MM, Robins-Browne RM, Holt KE. 2015. EcOH: in silico serotyping of E. coli from short read data. bioRxiv doi: 10.1099/mgen.0.000064.
38. Ingle DJ, Tauschek M, Edwards DJ, Hocking DM, Pickard DJ, Azzopardi KI, Amarasena T, Bennett-Wood V, Pearson JS, Tamboura B, et al. 2016. Evolution of atypical enteropathogenic E. coli by repeated acquisition of LEE pathogenicity island variants. Nat Microbiol 1: 15010.
39. Inouye M, Dashnow H, Raven LA, Schultz MB, Pope BJ, Tomita T, Zobel J, Holt KE. 2014. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 6: 90.
40. Ironmonger D, Edeghere O, Bains A, Loy R, Woodford N, Hawkey PM. 2015. Surveillance of antibiotic susceptibility of urinary tract pathogens for a population of 5.6 million over 4 years. J Antimicrob Chemother 70: 1744-1750.
41. 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.
42. Johnson JR, Delavari P, Kuskowski M, Stell AL. 2001. Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coli. J Infect Dis 183: 78-88.
43. Johnson JR, Tchesnokova V, Johnston B, Clabots C, Roberts PL, Billig M, Riddell K, Rogers P, Qin X, Butler-Wu S, et al. 2013. Abrupt emergence of a single dominant multidrug-resistant strain of Escherichia coli. J Infect Dis 207: 919-928.
44. 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.
45. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing S. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
46. Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, et al. 2016. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 16: 161-168.
47. Mellies JL, Navarro-Garcia F, Okeke I, Frederickson J, Nataro JP, Kaper JB. 2001. espC pathogenicity island of enteropathogenic Escherichia coli encodes an enterotoxin. Infect Immun 69: 315-324.
48. Miajlovic H, Mac Aogain M, Collins CJ, Rogers TR, Smith SG. 2016. Characterization of Escherichia coli bloodstream isolates associated with mortality. J Med Microbiol 65: 71-79.
49. Nicolas-Chanoine MH, Bertrand X, Madec JY. 2014. Escherichia coli ST131, an intriguing clonal group. Clin Microbiol Rev 27: 543-574.
50. Olesen B, Frimodt-Moller J, Leihof RF, Struve C, Johnston B, Hansen DS, Scheutz F, Krogfelt KA, Kuskowski MA, Clabots C, et al. 2014. Temporal trends in antimicrobial resistance and virulence-associated traits within Escherichia coli sequence type 131 clonal group and its H30 and H30-Rx subclones, 1968-2011. Antimicrob Agents Chemother 58: 6886-6895.
51. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MT, Fookes M, Falush D, Keane JA, Parkhill J. 2015. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31: 3691-3693.
52. Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T, Keane JA, Harris SR. 2016a. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microbial Genomics 2: doi: 10.1099/mgen.1090.000056.
53. Page AJ, Taylor B, Keane JA. 2016b. Multilocus sequence typing by blast from de novo assemblies against PubMLST. J Open Source Softw doi: 10.21105/joss.00118.
54. Petty NK, Ben Zakour NL, Stanton-Cook M, Skippington E, Totsika M, Forde BM, Phan MD, Gomes Moriel D, Peters KM, Davies M, et al. 2014. Global dissemination of a multidrug resistant Escherichia coli clone. Proc Natl Acad Sci 111: 5694-5699.
55. 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.
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-β-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. MBio 4: e00377-13.
57. R Core Team. 2015. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.Rproject. org/.
58. Rasko DA, Rosovitz MJ, Myers GS, Mongodin EF, Fricke WF, 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.
59. Reynolds R, Hope R, Williams L, Surveillance BWPoR. 2008. Survey, laboratory and statistical methods for the BSAC Resistance Surveillance Programmes. J Antimicrob Chemother 62(Suppl 2): i15-ii28.
60. Salipante SJ, Roach DJ, Kitzman JO, Snyder MW, Stackhouse B, Butler-Wu SM, Lee C, Cookson BT, Shendure J. 2015. Large-scale genomic sequencing of extraintestinal pathogenic Escherichia coli strains. Genome Res 25: 119-128.
61. Sana TG, Flaugnatti N, Lugo KA, Lam LH, Jacobson A, Baylot V, Durand E, Journet L, Cascales E, Monack DM. 2016. Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut. Proc Natl Acad Sci 113: E5044-E5051.
62. Schmidt H, Hensel M. 2004. Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev 17: 14-56.
63. Seemann T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30: 2068-2069.
64. Serapio-Palacios A, Navarro-Garcia F. 2016. EspC, an autotransporter protein secreted by enteropathogenic Escherichia coli, causes apoptosis and necrosis through caspase and calpain activation, including direct procaspase-3 cleavage. MBio 7: e00479-16.
65. Skov RL, Monnet DL. 2016. Plasmid-mediated colistin resistance (mcr-1 gene): three months later, the story unfolds. Euro Surveill 21: 30155.
66. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
67. Stein M, Kenny B, Stein MA, Finlay BB. 1996. Characterization of EspC, a 110-kilodalton protein secreted by enteropathogenic Escherichia coli which is homologous to members of the immunoglobulin A proteaselike family of secreted proteins. J Bacteriol 178: 6546-6554.
68. Stoesser N, Sheppard AE, Pankhurst L, De Maio N, Moore CE, Sebra R, Turner P, Anson LW, Kasarskis A, Batty EM, et al. 2016. Evolutionary history of the global emergence of the Escherichia coli epidemic clone ST131. MBio 7: e02162-15.
69. Tan A, Petty NK, Hocking D, Bennett-Wood V, Wakefield M, Praszkier J, Tauschek M, Yang J, Robins-Browne R. 2015. Evolutionary adaptation of an AraC-like regulatory protein in Citrobacter rodentium and Escherichia species. Infect Immun 83: 1384-1395.
70. To TH, Jung M, Lycett S, Gascuel O. 2016. Fast dating using least-squares criteria and algorithms. Syst Biol 65: 82-97.
71. Totsika M, Beatson SA, Sarkar S, Phan MD, Petty NK, Bachmann N, Szubert M, Sidjabat HE, Paterson DL, Upton M, et al. 2011. Insights into a multidrug resistant Escherichia coli pathogen of the globally disseminated ST131 lineage: genome analysis and virulence mechanisms. PLoS One 6: e26578.
72. von Mentzer A, Connor TR, Wieler LH, Semmler T, Iguchi A, Thomson NR, Rasko DA, Joffre E, Corander J, Pickard D, et al. 2014. Identification of enterotoxigenic Escherichia coli (ETEC) clades with long-term global distribution. Nat Genet 46: 1321-1326.
73. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, et al. 2006. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60: 1136-1151.
74. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV. 2012. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67: 2640-2644.
75. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829.
76. Zhang C, Xu X, Pu S, Huang S, Sun J, Yang S, Zhang L. 2014. Characterization of carbapenemases, extended spectrum β-lactamases, quinolone resistance and aminoglycoside resistance determinants in carbapenem-non-susceptible Escherichia coli from a teaching hospital in Chongqing, Southwest China. Infect Genet Evol 27: 271-276.
77. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. 2011. PHAST: a fast phage search tool. Nucleic Acids Res 39(Web Server issue): W347-W352.