1887

Abstract

Sequence type (ST)73 has emerged as one of the most frequently isolated extraintestinal pathogenic . To examine the localized diversity of ST73 clonal groups, including their mobile genetic element profile, we sequenced the genomes of 16 multiple-drug resistant ST73 isolates from patients with urinary tract infection from a single hospital in Sydney, Australia, between 2009 and 2011. Genome sequences were used to generate a SNP-based phylogenetic tree to determine the relationship of these isolates in a global context with ST73 sequences (=210) from public databases. There was no evidence of a dominant outbreak strain of ST73 in patients from this hospital, rather we identified at least eight separate groups, several of which reoccurred, over a 2 year period. The inferred phylogeny of all ST73 strains (=226) including the ST73 clone D i2 reference genome shows high bootstrap support and clusters into four major groups that correlate with serotype. The Sydney ST73 strains carry a wide variety of virulence-associated genes, but the presence of , and several iron-acquisition operons was notable.

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2019-02-27
2024-03-28
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References

  1. Gibreel TM, Dodgson AR, Cheesbrough J, Fox AJ, Bolton FJ et al. Population structure, virulence potential and antibiotic susceptibility of uropathogenic Escherichia coli from Northwest England. J Antimicrob Chemother 2012; 67:346–356 [View Article][PubMed]
    [Google Scholar]
  2. Kim S, Sung JY, Cho HH, Kwon KC, Koo SH. Characteristics of the molecular epidemiology of CTX-M-producing Escherichia coli isolated from a tertiary hospital in Daejeon, Korea. J Microbiol Biotechnol 2016; 26:1643–1649 [View Article][PubMed]
    [Google Scholar]
  3. Manges AR, Johnson JR. Reservoirs of extraintestinal pathogenic Escherichia coli . Microbiol Spectr 2015; 3:UTI-0006-2012 [View Article][PubMed]
    [Google Scholar]
  4. Olesen B, Scheutz F, Menard M, Skov MN, Kolmos HJ et al. Three-decade epidemiological analysis of Escherichia coli O15:K52:H1. J Clin Microbiol 2009; 47:1857–1862 [View Article][PubMed]
    [Google Scholar]
  5. Yun KW, Kim DS, Kim W, Lim IS. Molecular typing of uropathogenic Escherichia coli isolated from Korean children with urinary tract infection. Korean J Pediatr 2015; 58:20–27 [View Article][PubMed]
    [Google Scholar]
  6. Johnson JR, Thuras P, Johnston BD, Weissman SJ, Limaye AP et al. The pandemic H30 subclone of Escherichia coli sequence type 131 is associated with persistent infections and adverse outcomes independent from its multidrug resistance and associations with compromised hosts. Clin Infect Dis 2016; 62:1529–1536 [View Article][PubMed]
    [Google Scholar]
  7. Pitout JD. Extraintestinal pathogenic Escherichia coli: a combination of virulence with antibiotic resistance. Front Microbiol 2012; 3:9 [View Article][PubMed]
    [Google Scholar]
  8. Wirth T, Falush D, Lan R, Colles F, Mensa P et al. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 2006; 60:1136–1151 [View Article][PubMed]
    [Google Scholar]
  9. Phan MD, Peters KM, Sarkar S, Lukowski SW, Allsopp LP et al. The serum resistome of a globally disseminated multidrug resistant uropathogenic Escherichia coli clone. PLoS Genet 2013; 9:e1003834 [View Article][PubMed]
    [Google Scholar]
  10. de Kraker ME, Jarlier V, Monen JC, Heuer OE, van de Sande N et al. The changing epidemiology of bacteraemias in Europe: trends from the European Antimicrobial Resistance Surveillance System. Clin Microbiol Infect 2013; 19:860–868 [View Article][PubMed]
    [Google Scholar]
  11. Alhashash F, Wang X, Paszkiewicz K, Diggle M, Zong Z et al. 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 2016; 71:339–343 [View Article][PubMed]
    [Google Scholar]
  12. de Souza da-Silva AP, de Sousa VS, Martins N, da Silva Dias RC, Bonelli RR et al. Escherichia coli sequence type 73 as a cause of community acquired urinary tract infection in men and women in Rio de Janeiro, Brazil. Diagn Microbiol Infect Dis 2017; 88:69–74 [View Article][PubMed]
    [Google Scholar]
  13. Miajlovic H, Aogáin MM, Collins CJ, Rogers TR, Smith SG. Characterization of Escherichia coli bloodstream isolates associated with mortality. J Med Microbiol 2016; 65:71–79 [View Article][PubMed]
    [Google Scholar]
  14. Yahiaoui M, Robin F, Bakour R, Hamidi M, Bonnet R et al. Antibiotic resistance, virulence, and genetic background of community-acquired uropathogenic Escherichia coli from Algeria. Microb Drug Resist 2015; 21:516–526 [View Article][PubMed]
    [Google Scholar]
  15. Clermont O, Gordon D, Denamur E. Guide to the various phylogenetic classification schemes for Escherichia coli and the correspondence among schemes. Microbiology 2015; 161:980–988 [View Article][PubMed]
    [Google Scholar]
  16. Riley LW. Pandemic lineages of extraintestinal pathogenic Escherichia coli . Clin Microbiol Infect 2014; 20:380–390 [View Article][PubMed]
    [Google Scholar]
  17. Bengtsson S, Naseer U, Sundsfjord A, Kahlmeter G, Sundqvist M. Sequence types and plasmid carriage of uropathogenic Escherichia coli devoid of phenotypically detectable resistance. J Antimicrob Chemother 2012; 67:69–73 [View Article][PubMed]
    [Google Scholar]
  18. Kahlmeter G, Åhman J, Matuschek E. Antimicrobial resistance of Escherichia coli causing uncomplicated urinary tract infections: a European update for 2014 and comparison with 2000 and 2008. Infect Dis Ther 2015; 4:417–423 [View Article][PubMed]
    [Google Scholar]
  19. Gillings MR, Gaze WH, Pruden A, Smalla K, Tiedje JM et al. Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J 2015; 9:1269–1279 [View Article][PubMed]
    [Google Scholar]
  20. Bell SM, Pham JN, Rafferty DL, Allerton JK. Antibiotic Susceptibility Testing by the CDS Method: A Manual for Medical and Veterinary Laboratories, 8th edn. vol. 2016. Kogarah: South Eastern Area Laboratory Services; 2016
    [Google Scholar]
  21. Coil D, Jospin G, Darling AE. A5-MiSeq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics 2015; 31:587–589 [View Article][PubMed]
    [Google Scholar]
  22. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article][PubMed]
    [Google Scholar]
  23. Inouye M, Dashnow H, Raven LA, Schultz MB, Pope BJ et al. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 2014; 6:90 [View Article][PubMed]
    [Google Scholar]
  24. Chen L, Yang J, Yu J, Yao Z, Sun L et al. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 2005; 33:D325–D328 [View Article][PubMed]
    [Google Scholar]
  25. Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M et al. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 2014; 58:212–220 [View Article][PubMed]
    [Google Scholar]
  26. Minogue TD, Daligault HA, Davenport KW, Bishop-Lilly KA, Broomall SM et al. Complete genome assembly of Escherichia coli ATCC 25922, a serotype O6 reference strain. Genome Announc 2014; 2:e00969-14 [View Article][PubMed]
    [Google Scholar]
  27. Reeves PR, Liu B, Zhou Z, Li D, Guo D et al. Rates of mutation and host transmission for an Escherichia coli clone over 3 years. PLoS One 2011; 6:e26907 [View Article][PubMed]
    [Google Scholar]
  28. Reister M, Hoffmeier K, Krezdorn N, Rotter B, Liang C et al. Complete genome sequence of the gram-negative probiotic Escherichia coli strain Nissle 1917. J Biotechnol 2014; 187:106–107 [View Article][PubMed]
    [Google Scholar]
  29. Zdziarski J, Brzuszkiewicz E, Wullt B, Liesegang H, Biran D et al. Host imprints on bacterial genomes-rapid, divergent evolution in individual patients. PLoS Pathog 2010; 6:e1001078 [View Article][PubMed]
    [Google Scholar]
  30. Welch RA, Burland V, Plunkett G, Redford P, Roesch P et al. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli . Proc Natl Acad Sci USA 2002; 99:17020–17024 [View Article][PubMed]
    [Google Scholar]
  31. Dallman TJ, Byrne L, Ashton PM, Cowley LA, Perry NT et al. Whole-genome sequencing for national surveillance of Shiga toxin-producing Escherichia coli O157. Clin Infect Dis 2015; 61:305–312 [View Article][PubMed]
    [Google Scholar]
  32. Dunitz MI, Coil DA, Jospin G, Eisen JA, Adams JY. Draft genome sequences of Escherichia coli strains isolated from septic patients. Genome Announc 2014; 2:e01278-14 [View Article][PubMed]
    [Google Scholar]
  33. Earle SG, Wu CH, Charlesworth J, Stoesser N, Gordon NC et al. Identifying lineage effects when controlling for population structure improves power in bacterial association studies. Nat Microbiol 2016; 1:16041 [View Article]
    [Google Scholar]
  34. Kluytmans-van den Bergh MF, Rossen JW, Bruijning-Verhagen PC, Bonten MJ, Friedrich AW et al. Whole-genome multilocus sequence typing of extended-spectrum-beta-lactamase-producing enterobacteriaceae. J Clin Microbiol 2016; 54:2919–2927 [View Article][PubMed]
    [Google Scholar]
  35. Pesesky MW, Hussain T, Wallace M, Wang B, Andleeb S et al. KPC and NDM-1 genes in related Enterobacteriaceae strains and plasmids from Pakistan and the United States. Emerg Infect Dis 2015; 21:1034–1037 [View Article][PubMed]
    [Google Scholar]
  36. Roach DJ, Burton JN, Lee C, Stackhouse B, Butler-Wu SM et al. A year of infection in the intensive care unit: prospective whole genome sequencing of bacterial clinical isolates reveals cryptic transmissions and novel microbiota. PLoS Genet 2015; 11:e1005413 [View Article][PubMed]
    [Google Scholar]
  37. Salipante SJ, Roach DJ, Kitzman JO, Snyder MW, Stackhouse B et al. Large-scale genomic sequencing of extraintestinal pathogenic Escherichia coli strains. Genome Res 2015; 25:119–128 [View Article][PubMed]
    [Google Scholar]
  38. Toro M, Cao G, Rump L, Nagaraja TG, Meng J et al. Genome sequences of 64 non-O157:H7 Shiga toxin-producing Escherichia coli strains. Genome Announc 2015; 3:e01067-15 [View Article][PubMed]
    [Google Scholar]
  39. Barton BM, Harding GP, Zuccarelli AJ. A general method for detecting and sizing large plasmids. Anal Biochem 1995; 226:235–240 [View Article][PubMed]
    [Google Scholar]
  40. Partridge SR, Zong Z, Iredell JR. Recombination in IS26 and Tn2 in the evolution of multiresistance regions carrying blaCTX-M-15 on conjugative IncF plasmids from Escherichia coli . Antimicrob Agents Chemother 2011; 55:4971–4978 [View Article][PubMed]
    [Google Scholar]
  41. Koeleman JG, Stoof J, van der Bijl MW, Vandenbroucke-Grauls CM, Savelkoul PH. Identification of epidemic strains of Acinetobacter baumannii by integrase gene PCR. J Clin Microbiol 2001; 39:8–13 [View Article][PubMed]
    [Google Scholar]
  42. Darling AE, Jospin G, Lowe E, Matsen FA, Bik HM et al. PhyloSift: phylogenetic analysis of genomes and metagenomes. PeerJ 2014; 2:e243 [View Article][PubMed]
    [Google Scholar]
  43. Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J et al. Rapid pneumococcal evolution in response to clinical interventions. Science 2011; 331:430–434 [View Article][PubMed]
    [Google Scholar]
  44. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  45. Nesta B, Spraggon G, Alteri C, Moriel DG, Rosini R et al. FdeC, a novel broadly conserved Escherichia coli adhesin eliciting protection against urinary tract infections. MBio 2012; 3:e00010-12 [View Article][PubMed]
    [Google Scholar]
  46. Ladomersky E, Petris MJ. Copper tolerance and virulence in bacteria. Metallomics 2015; 7:957–964 [View Article][PubMed]
    [Google Scholar]
  47. Baker-Austin C, Wright MS, Stepanauskas R, Mcarthur JV. Co-selection of antibiotic and metal resistance. Trends Microbiol 2006; 14:176–182 [View Article][PubMed]
    [Google Scholar]
  48. Nakaya R, Nakamura A, Murata Y. Resistance transfer agents in Shigella. Biochem Biophys Res Commun 1960; 3:654–659 [View Article][PubMed]
    [Google Scholar]
  49. García V, García P, Rodríguez I, Rodicio R, Rodicio MR. The role of IS26 in evolution of a derivative of the virulence plasmid of Salmonella enterica serovar Enteritidis which confers multiple drug resistance. Infect Genet Evol 2016; 45:246–249 [View Article][PubMed]
    [Google Scholar]
  50. Broom JE, Hill DF, Hughes G, Jones WA, McNaughton JC et al. Sequence of a transposon identified as Tn1000 (gamma delta). DNA Seq 1995; 5:185–189 [View Article][PubMed]
    [Google Scholar]
  51. Petty NK, Ben Zakour NL, Stanton-Cook M, Skippington E, Totsika M et al. Global dissemination of a multidrug resistant Escherichia coli clone. Proc Natl Acad Sci USA 2014; 111:5694–5699 [View Article][PubMed]
    [Google Scholar]
  52. Price LB, Johnson JR, Aziz M, Clabots C, Johnston B et al. The epidemic of extended-spectrum-β-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. MBio 2013; 4:e00377-13 [View Article][PubMed]
    [Google Scholar]
  53. Dawes FE, Kuzevski A, Bettelheim KA, Hornitzky MA, Djordjevic SP et al. Distribution of class 1 integrons with IS26-mediated deletions in their 3'-conserved segments in Escherichia coli of human and animal origin. PLoS One 2010; 5:e12754 [View Article][PubMed]
    [Google Scholar]
  54. Roy Chowdhury P, Charles IG, Djordjevic SP. A role for Tn6029 in the evolution of the complex antibiotic resistance gene loci in genomic island 3 in enteroaggregative hemorrhagic Escherichia coli O104:H4. PLoS One 2015; 10:e0115781 [View Article][PubMed]
    [Google Scholar]
  55. Mckinnon J, Roy Chowdhury P, Djordjevic SP. Genomic analysis of multidrug-resistant Escherichia coli ST58 causing urosepsis. Int J Antimicrob Agents 2018; 52:430–435 [View Article][PubMed]
    [Google Scholar]
  56. Rodríguez I, Rodicio MR, Herrera-León S, Echeita A, Mendoza MC. Class 1 integrons in multidrug-resistant non-typhoidal Salmonella enterica isolated in Spain between 2002 and 2004. Int J Antimicrob Agents 2008; 32:158–164 [View Article][PubMed]
    [Google Scholar]
  57. Cunha MPV, Saidenberg AB, Moreno AM, Ferreira AJP, Vieira MAM et al. Pandemic extra-intestinal pathogenic Escherichia coli (ExPEC) clonal group O6-B2-ST73 as a cause of avian colibacillosis in Brazil. PLoS One 2017; 12:e0178970 [View Article][PubMed]
    [Google Scholar]
  58. Liu X, Thungrat K, Boothe DM. Multilocus sequence typing and virulence profiles in uropathogenic Escherichia coli isolated from cats in the United States. PLoS One 2015; 10:e0143335 [View Article][PubMed]
    [Google Scholar]
  59. Yun KW, Kim HY, Park HK, Kim W, Lim IS. Virulence factors of uropathogenic Escherichia coli of urinary tract infections and asymptomatic bacteriuria in children. J Microbiol Immunol Infect 2014; 47:455–461 [View Article][PubMed]
    [Google Scholar]
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