Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Species Transferability of Klebsiella pneumoniae Carbapenemase-2 Isolated from a High-Risk Clone of Escherichia coli ST410

  • Lee, Miyoung (Department of Microbiology Pukyoung National University) ;
  • Choi, Tae-Jin (Department of Microbiology Pukyoung National University)
  • Received : 2019.12.29
  • Accepted : 2020.05.19
  • Published : 2020.07.28
Download PDF
⟨ Previous Next ⟩

Abstract

Sequence type 410 (ST410) of Escherichia coli is an extraintestinal pathogen associated with multi drug resistance. In this study, we aimed to investigate the horizontal propagation pathway of a high-risk clone of E. coli ST410 that produces Klebsiella pneumoniae carbapenemase (KPC). blaKPC-encoding E. coli and K. pneumoniae isolates were evaluated, and complete sequencing and comparative analysis of blaKPC-encoding plasmids from E. coli and K. pneumoniae, antimicrobial susceptibility tests, polymerase chain reaction, multilocus sequence typing, and conjugal transfer of plasmids were performed. Whole-genome sequencing was performed for plasmids mediating KPC-2 production in E. coli and K. pneumoniae clinical isolates. Strains E. coli CPEc171209 and K. pneumoniae CPKp171210 were identified as ST410 and ST307, respectively. CPEc171209 harbored five plasmids belonging to serotype O8:H21, which is in the antimicrobial-resistant clade C4/H24. The CPKp171210 isolate harbored three plasmids. Both strains harbored various additional antimicrobial resistance genes. The IncX3 plasmid pECBHS_9_5 harbored blaKPC-2 within a truncated Tn4401a transposon, which also contains blaSHV-182 with duplicated conjugative elements. This plasmid displayed 100% identity with the IncX3 plasmid pKPBHS_10_3 from the K. pneumoniae CPKp171210 ST307 strain. The genes responsible for the conjugal transfer of the IncX3 plasmid included tra/trb clusters and pil genes coding the type IV pilus. ST410 can be transmitted between patients, posing an elevated risk in clinical settings. The emergence of a KPC-producing E. coli strain (ST410) is concerning because the blaKPC-2-bearing plasmids may carry treatment resistance across species barriers. Transgenic translocation occurs among carbapenem-resistant bacteria, which may spread rapidly via horizontal migration.

Keywords

References

  1. Rhomberg PR, Deshpande LM, Kirby JT, Jones RN. 2007. Activity of meropenem as serine carbapenemases evolve in US Medical Centers: monitoring report from the MYSTIC Program (2006). Diagn. Microbiol. Infect. Dis. 59: 425-432. https://doi.org/10.1016/j.diagmicrobio.2007.05.009
  2. Munoz-Price LS, Poirel L, Bonomo RA, Schwaber MJ, Daikos GL, Cormican M, et al. 2013. Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases. Lancet Infect. Dis. 13: 785-796. https://doi.org/10.1016/S1473-3099(13)70190-7
  3. Pitout JD, Nordmann P, Poirel L. 2015. Carbapenemase-producing Klebsiella pneumoniae, a key pathogen set for global nosocomial dominance. Antimicrob. Agents Chemother. 59: 5873-5884. https://doi.org/10.1128/AAC.01019-15
  4. Adler A, Miller-Roll T, Assous MV, Geffen Y, Paikin S, Schwartz D, et al. 2015. A multicenter study of the clonal structure and resistance mechanism of KPC-producing Escherichia coli isolates in Israel. Clin. Microbiol. Infect. 21: 230-235. https://doi.org/10.1016/j.cmi.2014.10.008
  5. Piazza A, Caltagirone M, Bitar I, Nucleo E, Spalla M, Fogato E, et al. 2016. Emergence of Escherichia coli sequence type 131 (ST131) and ST3948 with KPC-2, KPC-3 and KPC-8 carbapenemases from a long-term care and rehabilitation facility (LTCRF) in northern Italy. Adv. Exp. Med. Biol. 901: 77-89.
  6. Chavda KD, Chen L, Jacobs MR, Bonomo RA, Kreiswirth BN. 2016. Molecular diversity and plasmid analysis of KPC-producing Escherichia coli. Antimicrob. Agents Chemother. 60: 4073-4081. https://doi.org/10.1128/AAC.00452-16
  7. Xu G, Jiang Y, An W, Wang H, Zhang X. 2015. Emergence of KPC-2-producing Escherichia coli isolates in an urban river in Harbin, China. World J. Microbiol. Biotechnol. 31: 1443-1450. https://doi.org/10.1007/s11274-015-1897-z
  8. Schaufler K, Semmler T, Wieler LH, Wohrmann M, Baddam R, Ahmed N, et al. 2016. Clonal spread and interspecies transmission of clinically relevant ESBL-producing Escherichia coli of ST410-another successful pandemic clone? FEMS Microbiol. Ecol. 92: fiv155. https://doi.org/10.1093/femsec/fiv155
  9. Falgenhauer L, Imirzalioglu C, Ghosh H, Gwozdzinski K, Schmiedel J, Gentil K, et al. 2016. Circulation of clonal populations of fluoroquinolone-resistant CTX-M-15-producing Escherichia coli ST410 in humans and animals in Germany. Int. J. Antimicrob. Agents 47: 457-465. https://doi.org/10.1016/j.ijantimicag.2016.03.019
  10. Roer L, Overballe-Petersen S, Hansen F, Schonning K, Wang M, Roder BL, et al. 2018. Escherichia coli sequence type 410 is causing new international high-risk clones. mSphere 3: e00337-18.
  11. Solgi H, Badmasti F, Aminzadeh Z, Giske CG, Pourahmad M, Vaziri F, et al. 2017. Molecular characterization of intestinal carriage of carbapenem-resistant Enterobacteriaceae among inpatients at two Iranian university hospitals: first report of co-production of blaNDM-7 and blaOXA-48. Eur. J. Clin. Microbiol. Infect. Dis. 36: 2127-2135. https://doi.org/10.1007/s10096-017-3035-3
  12. Ohno Y, Nakamura A, Hashimoto E, Matsutani H, Abe N, Fukuda et al. 2017. Molecular epidemiology of carbapenemase-producing Enterobacteriaceae in a primary care hospital in Japan, 2010-2013. J. Infect. Chemother. 23: 224-229. https://doi.org/10.1016/j.jiac.2016.12.013
  13. He S, Chandler M, Varani AM, Hickman AB, Dekker JP, Dyda F. 2016. Mechanisms of evolution in high-consequence drug resistance plasmids. MBio 7: e01987-16.
  14. Mouloudi E, Protonotariou E, Zagorianou A, Iosifidis E, Karapanagiotou A, Giasnetsova T, et al. 2010. Bloodstream infections caused by metallo-beta-lactamase/Klebsiella pneumoniae carbapenemase-producing K. pneumoniae among intensive care unit patients in Greece: risk factors for infection and impact of type of resistance on outcomes. Infect. Control Hosp. Epidemiol. 31: 1250-1256. https://doi.org/10.1086/657135
  15. Walsh TR, Weeks J, Livermore DM, Toleman MA. 2011. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect. Dis. 11: 355-362. https://doi.org/10.1016/S1473-3099(11)70059-7
  16. Copur Cicek A, Ozad Duzgun A, Saral A, Sandalli C. 2014. Determination of a novel integron-located variant (blaOXA-320) of Class D $\beta$-lactamase in Proteus mirabilis. J. Basic Microbiol. 54:1030-1035. https://doi.org/10.1002/jobm.201300264
  17. Clinical and Laboratory Standards Institute. 2018. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Clinical and Laboratory Standards Institute, Wayne, P. A.
  18. EUCAST. Antimicrobial susceptibility testing of bacteria. Available from http://www.eucast.org/ast_of_bacteria/ (Updated on Jan 2017). Accessed April 30, 2019.
  19. Jeong S, Kim JO, Jeong SH, Bae IK, Song W. 2015. Evaluation of peptide nucleic acid-mediated multiplex real-time PCR kits for rapid detection of carbapenemase genes in gram-negative clinical isolates. J. Microbiol. Methods 113: 4-9. https://doi.org/10.1016/j.mimet.2015.03.019
  20. Perez-Perez FJ, Hanson ND. 2002. Detection of plasmid-mediated AmpC b-lactamase genes in clinical isolates by using multiplex PCR. J. Clin. Microbiol. 40: 2153-2162. https://doi.org/10.1128/JCM.40.6.2153-2162.2002
  21. Ryoo NH, Kim EC, Hong SG, Park YJ, Lee K, Bae IK, et al. 2005. Dissemination of SHV-12 and CTX-M-type extended-spectrum beta-lactamases among clinical isolates of Escherichia coli and Klebsiella pneumoniae and emergence of GES-3 in Korea. J. Antimicrob. Chemother. 56: 698-702. https://doi.org/10.1093/jac/dki324
  22. Yamane K, Wachino J, Suzuki S, Arakawa Y. 2008. Plasmid-mediated qepA gene among Escherichia coli clinical isolates from Japan. Antimicrob. Agents Chemother. 52: 1564-1566. https://doi.org/10.1128/AAC.01137-07
  23. Landman D, Bratu S, Quale J. 2009. Contribution of ompK36 to carbapenem susceptibility in KPC-producing Klebsiella pneumoniae. J. Med. Microbial. 58: 1303-1308. https://doi.org/10.1099/jmm.0.012575-0
  24. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, et al. 2006. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol. Microbiol. 60: 1136-1151. https://doi.org/10.1111/j.1365-2958.2006.05172.x
  25. Diancourt L, Passet V, Verhoef J, Grimont PA, Brisse S. 2005. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J. Clin. Microbiol. 43: 4178-182. https://doi.org/10.1128/JCM.43.8.4178-4182.2005
  26. Jeong SH, Lee KM, Lee J, Bae IK, Kim JS, Kim HS, et al. 2015. Clonal and horizontal spread of the blaOXA-232 gene among Enterobacteriaceae in a Korean hospital. Diagn. Microbiol. Infect. Dis. 82: 70-72. https://doi.org/10.1016/j.diagmicrobio.2015.02.001
  27. Naas T, Cuzon G, Truong HV, Nordmann P. 2012. Role of ISKpn7 and deletions in blaKPC gene expression. Antimicrob. Agents Chemother. 56: 4753-4759. https://doi.org/10.1128/AAC.00334-12
  28. Yang Q, Fang L, Fu Y, Du X, Shen Y, Yu Y. 2015. Dissemination of NDM-1-producing Enterobacteriaceae mediated by the IncX3-type plasmid. PLoS One 10: e0129454. https://doi.org/10.1371/journal.pone.0129454
  29. Chen L, Chavda KD, Melano RG, Jacobs MR, Levi MH, Bonomo RA, et al. 2013. Complete sequence of a bla (KPC-2)-harboring IncFII (K1) plasmid from a Klebsiella pneumoniae sequence type 258 strain. Antimicrob. Agents. Chemother. 57: 1542-1545. https://doi.org/10.1128/AAC.02332-12
  30. Kassis-Chikhani N, Frangeul L, Drieux L, Sengelin C, Jarlier V, Brisse S, et al. 2013. Complete nucleotide sequence of the first KPC-2- and SHV-12-encoding IncX plasmid, pKpS90, from Klebsiella pneumoniae. Antimicrob. Agents Chemother. 57: 618-620. https://doi.org/10.1128/AAC.01712-12
  31. Naas T, Cuzon G, Villegas MV, Lartigue MF, Quinn JP, Nordmann P. 2008. Genetic structures at the origin of acquisition of the beta-lactamase blaKPC gene. Antimicrob. Agents Chemother. 52: 1257-1263. https://doi.org/10.1128/AAC.01451-07
  32. Jeong S, Kim JO, Yoon EJ, Bae IK, Lee W, Lee H, et al. 2018. Extensively drug-resistant Escherichia coli sequence type 1642 carrying an IncX3 plasmid containing the blaKPC-2 gene associated with transposon Tn4401a. Ann. Lab. Med. 38: 17-22. https://doi.org/10.3343/alm.2018.38.1.17
  33. Tseng TT, Gratwick KS, Kollman J, Park D, Nies DH, Goffeau A, et al. 1999. The RND permease superfamily: an ancient, ubiquitous, and diverse family that includes human disease and development protein. J. Mol. Microbiol. Biotechnol. 1: 107-125.
  34. Nies DH. 2003. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol. Rev. 27: 313-339. https://doi.org/10.1016/S0168-6445(03)00048-2
  35. Franke S, Grass G, Nies DH. 2001. The product of the ybdE gene of the Escherichia coli chromosome is involved in detoxification of silver ions. Microbiology 147: 965-972. https://doi.org/10.1099/00221287-147-4-965
  36. Franke S, Grass G, Rensing C, Nies DH. 2003. Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J. Bacteriol. 185: 3804-3812. https://doi.org/10.1128/JB.185.13.3804-3812.2003

Cited by

  1. Complete Genome Sequences of Two Novel KPC-2-Producing IncU Multidrug-Resistant Plasmids From International High-Risk Clones of Escherichia coli in China vol.12, 2020, https://doi.org/10.3389/fmicb.2021.698478