1887

Abstract

Extended-spectrum β-lactamase (ESBL)-producing extraintestinal pathogenic (ExPEC) sequence type ST131 is pandemic, and it is the major contributor to antibiotic resistance in . Despite its epidemiological superiority, the physiological reasons that decipher its success remain elusive. We aimed to compare the adhesion, invasion and motility potential of ST131 versus other lineages.

In this comparative study, 14 ESBL-producing ExPEC community-onset bacteremia isolates were chosen from a reported clinical collection (Karfunkel D, Carmeli Y, Chmelnitsky I, Kotlovsky T, Navon-Venezia S. 2013;32:513–521). Isolates were divided into two groups, ST131 (=7) and ‘non-ST131’, sporadic sequence types (STs) (=7). Virulence and adhesion genes were screened by PCR in all isolates. Virotyping and serotyping were performed for ST131 isolates. Adhesion and invasion to Caco-2 epithelial cells, and motility on semi-solid agar were quantified and compared between the two groups. Fluorescence microscopy using anti-LPS antibodies was used for visualization and confirmation of adhesion and invasion.

ST131 isolates belonged to the O25b:H4-B2 subclone. Two ST131 virotypes were found, A (two H30-Rx) and C (two H30-Rx and three H30 isolates). The average number of adhesion and virulence genes carried by ExPEC ST131 isolates and non-ST131 isolates was 5.3 and 3.7, respectively (<0.05). Group analysis showed that ST131 surpassed non-ST131 lineages in all three physiological properties: adherence (17.1 vs 13.1 %, <0.001), invasion (0.4 vs 0.17 %, <0.01), and swarming motility on all media tested (<0.05).

This study demonstrates ST131 superiority that may explain its improved gut-colonization and dissemination capabilities within the host. These insights are an important step in our understanding of ST131 epidemiological success.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000549
2017-09-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jmm/66/9/1350.html?itemId=/content/journal/jmm/10.1099/jmm.0.000549&mimeType=html&fmt=ahah

References

  1. Pitout JDD. Extraintestinal pathogenic Escherichia coli: a combination of virulence with antibiotic resistance. Front Microbiol 2012; 3:1–7 [View Article]
    [Google Scholar]
  2. Nicolas-Chanoine MH, Bertrand X, Madec JY. Escherichia coli ST131, an intriguing clonal group. Clin Microbiol Rev 2014; 27:543–574 [View Article][PubMed]
    [Google Scholar]
  3. Riley LW. Pandemic lineages of extraintestinal pathogenic Escherichia coli. Clin Microbiol Infect 2014; 20:380–390 [View Article][PubMed]
    [Google Scholar]
  4. Karfunkel D, Carmeli Y, Chmelnitsky I, Kotlovsky T, Navon-Venezia S. The emergence and dissemination of CTX-M-producing Escherichia coli sequence type 131 causing community-onset bacteremia in Israel. Eur J Clin Microbiol Infect Dis 2013; 32:513–521 [View Article][PubMed]
    [Google Scholar]
  5. López-Cerero L, Navarro MD, Bellido M, Martín-Peña A, Viñas L et al. Escherichia coli belonging to the worldwide emerging epidemic clonal group O25b/ST131: risk factors and clinical implications. J Antimicrob Chemother 2014; 69:809–814 [View Article][PubMed]
    [Google Scholar]
  6. Nicolas-Chanoine MH, Gruson C, Bialek-Davenet S, Bertrand X, Thomas-Jean F et al. 10-Fold increase (2006–11) in the rate of healthy subjects with extended-spectrum β-lactamase-producing Escherichia coli faecal carriage in a Parisian check-up centre. J Antimicrob Chemother 2013; 68:562–568 [View Article][PubMed]
    [Google Scholar]
  7. Kudinha T, Johnson JR, Andrew SD, Kong F, Anderson P et al. Escherichia coli sequence type 131 as a prominent cause of antibiotic resistance among urinary Escherichia coli isolates from reproductive-age women. J Clin Microbiol 2013; 51:3270–3276 [View Article][PubMed]
    [Google Scholar]
  8. Gibreel TM, Dodgson AR, Cheesbrough J, Bolton FJ, Fox AJ et al. High metabolic potential may contribute to the success of ST131 uropathogenic Escherichia coli. J Clin Microbiol 2012; 50:3202–3207 [View Article][PubMed]
    [Google Scholar]
  9. Johnson JR, Clermont O, Menard M, Kuskowski MA, Picard B et al. Experimental mouse lethality of Escherichia coli isolates, in relation to accessory traits, phylogenetic group, and ecological source. J Infect Dis 2006; 194:1141–1150 [View Article][PubMed]
    [Google Scholar]
  10. Chung HC, Lai CH, Lin JN, Huang CK, Liang SH et al. Bacteremia caused by extended-spectrum-β-lactamase-producing Escherichia coli sequence type ST131 and non-ST131 clones: comparison of demographic data, clinical features, and mortality. Antimicrob Agents Chemother 2012; 56:618–622 [View Article][PubMed]
    [Google Scholar]
  11. Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 2013; 5:58–65 [View Article][PubMed]
    [Google Scholar]
  12. Woodford N, Fagan EJ, Ellington MJ. Multiplex PCR for rapid detection of genes encoding CTX-M extended-spectrum β-lactamases. J Antimicrob Chemother 2006; 57:154–155 [View Article][PubMed]
    [Google Scholar]
  13. Clermont O, Dhanji H, Upton M, Gibreel T, Fox A et al. Rapid detection of the O25b-ST131 clone of Escherichia coli encompassing the CTX-M-15-producing strains. J Antimicrob Chemother 2009; 64:274–277 [View Article][PubMed]
    [Google Scholar]
  14. Beutin L, Strauch E, Zimmermann S, Kaulfuss S, Schaudinn C et al. Genetical and functional investigation of fliC genes encoding flagellar serotype H4 in wildtype strains of Escherichia coli and in a laboratory E. coli K-12 strain expressing flagellar antigen type H48. BMC Microbiol 2005; 5:4 [View Article][PubMed]
    [Google Scholar]
  15. Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999; 41:95–98
    [Google Scholar]
  16. Blanco J, Mora A, Mamani R, López C, Blanco M et al. Four main virotypes among extended-spectrum-β-lactamase-producing isolates of Escherichia coli O25b:H4-B2-ST131: bacterial, epidemiological, and clinical characteristics. J Clin Microbiol 2013; 51:3358–3367 [View Article][PubMed]
    [Google Scholar]
  17. Colpan A, Johnston B, Porter S, Clabots C, Anway R et al. Escherichia coli sequence type 131 (ST131) subclone H30 as an emergent multidrug-resistant pathogen among US veterans. Clin Infect Dis 2013; 57:1256–1265 [View Article][PubMed]
    [Google Scholar]
  18. Banerjee R, Robicsek A, Kuskowski MA, Porter S, Johnston BD et al. Molecular epidemiology of Escherichia coli sequence type 131 and its H30 and H30-Rx subclones among extended-spectrum-β-lactamase-positive and -negative E. coli clinical isolates from the Chicago region, 2007 to 2010. Antimicrob Agents Chemother 2013; 57:6385–6388 [View Article][PubMed]
    [Google Scholar]
  19. Johnson JR, Stell AL. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J Infect Dis 2000; 181:261–272 [View Article][PubMed]
    [Google Scholar]
  20. Lloyd SJ, Ritchie JM, Rojas-Lopez M, Blumentritt CA, Popov VL et al. A double, long polar fimbria mutant of Escherichia coli O157:H7 expresses curli and exhibits reduced in vivo colonization. Infect Immun 2012; 80:914–920 [View Article][PubMed]
    [Google Scholar]
  21. Blackburn D, Husband A, Saldaña Z, Nada RA, Klena J et al. Distribution of the Escherichia coli common pilus among diverse strains of human enterotoxigenic E. coli. J Clin Microbiol 2009; 47:1781–1784 [View Article][PubMed]
    [Google Scholar]
  22. Ewers C, Li G, Wilking H, Kiessling S, Alt K et al. Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they?. Int J Med Microbiol 2007; 297:163–176 [View Article][PubMed]
    [Google Scholar]
  23. Martinez JJ, Mulvey MA, Schilling JD, Pinkner JS, Hultgren SJ. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. Embo J 2000; 19:2803–2812 [View Article][PubMed]
    [Google Scholar]
  24. Lane MC, Lockatell V, Monterosso G, Lamphier D, Weinert J et al. Role of motility in the colonization of uropathogenic Escherichia coli in the urinary tract. Infect Immun 2005; 73:7644–7656 [View Article][PubMed]
    [Google Scholar]
  25. Nicolas-Chanoine MH, Blanco J, Leflon-Guibout V, Demarty R, Alonso MP et al. Intercontinental emergence of Escherichia coli clone O25:H4-ST131 producing CTX-M-15. J Antimicrob Chemother 2008; 61:273–281 [View Article][PubMed]
    [Google Scholar]
  26. Vimont S, Boyd A, Bleibtreu A, Bens M, Goujon JM et al. The CTX-M-15-producing Escherichia coli clone O25b: H4-ST131 has high intestine colonization and urinary tract infection abilities. PLoS One 2012; 7:e46547 [View Article][PubMed]
    [Google Scholar]
  27. Kalita A, Hu J, Torres AG. Recent advances in adherence and invasion of pathogenic Escherichia coli. Curr Opin Infect Dis 2014; 27:459–464 [View Article][PubMed]
    [Google Scholar]
  28. Ottemann KM, Miller JF. Roles for motility in bacterial-host interactions. Mol Microbiol 1997; 24:1109–1117 [View Article][PubMed]
    [Google Scholar]
  29. Klemm P, Hancock V, Schembri MA. Fimbrial adhesins from extraintestinal Escherichia coli. Environ Microbiol Rep 2010; 2:628–640 [View Article][PubMed]
    [Google Scholar]
  30. Kakkanat A, Totsika M, Schaale K, Duell BL, Lo AW et al. The role of H4 flagella in Escherichia coli ST131 virulence. Sci Rep 2015; 5:16149 [View Article][PubMed]
    [Google Scholar]
  31. Peirano G, Mulvey GL, Armstrong GD, Pitout JD. Virulence potential and adherence properties of Escherichia coli that produce CTX-M and NDM β-lactamases. J Med Microbiol 2013; 62:525–530 [View Article][PubMed]
    [Google Scholar]
  32. Yin X, Wheatcroft R, Chambers JR, Liu B, Zhu J et al. Contributions of O island 48 to adherence of enterohemorrhagic Escherichia coli O157:H7 to epithelial cells in vitro and in ligated pig ileal loops. Appl Environ Microbiol 2009; 75:5779–5786 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000549
Loading
/content/journal/jmm/10.1099/jmm.0.000549
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error