1887

Journal of Medical Microbiology logo

Volume 73, Issue 4

sequence type 147: a high-risk clone increasingly associated with plasmids carrying both resistance and virulence elements Open Access

Abstract

The first hybrid resistance/virulence plasmid, combining elements from virulence plasmids described in hypervirulent types of with those from conjugative resistance plasmids, was described in an isolate of sequence type (ST) 147 from 2016. Subsequently, this type has been increasingly associated with these plasmids.

The extent of carriage of hybrid virulence/resistance plasmids in nosocomial isolates of requires further investigation.

To describe the occurrence of virulence/resistance plasmids among isolates of received by the UK reference laboratory, particularly among representatives of ST147, and to compare their sequences.

Isolates received by the laboratory during 2022 and the first half of 2023 (=1278) were screened for virulence plasmids by PCR detection of / and typed by variable-number tandem repeat analysis. Twenty-nine representatives of ST147 (including a single-locus variant) from seven hospital laboratories were subjected to long-read nanopore sequencing using high-accuracy q20 chemistry to provide complete assemblies.

/ were detected in 110 isolates, of which 59 belonged to hypervirulent K1-ST23, K2-ST86 and K2-ST65/375. Of the remainder, representatives of ST147 formed the largest group, with 22 /-positive representatives (out of 47 isolates). Representatives were from 19 hospital laboratories, with /-positive isolates from 10. Nanopore sequencing of 29 representatives of ST147 divided them into those with no virulence plasmid (=12), those with non-New Delhi metallo-β-lactamase (NDM) virulence plasmids (=6) and those carrying (=9) or (=2) virulence plasmids. These plasmids were of IncFIB(pNDM-Mar)/IncHI1B(pNDM-MAR) replicon types. Most of the non-NDM virulence plasmids were highly similar to the originally described KpvST147L_NDM plasmid. Those carrying were highly similar to one another and to previously described plasmids in ST383 and carried an extensive array of resistance genes. Comparison of the fully assembled chromosomes indicated multiple introductions of ST147 in UK hospitals.

This study highlights the high proportion of representatives of ST147 that carry IncFIB(pNDM-Mar)/IncHI1B(pNDM-MAR) hybrid resistance virulence plasmids. It is important to be aware of the high probability that representatives of this type carry these plasmids combining resistance and virulence determinants and of the consequent increased risk to patients.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): hybrid plasmids , Klebsiella pneumoniae , nanopore sequencing , sequence type 147 and virulence
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001823
2024-04-17
2024-04-30
Loading full text...

Full text loading...

/deliver/fulltext/jmm/73/4/jmm001823.html?itemId=/content/journal/jmm/10.1099/jmm.0.001823&mimeType=html&fmt=ahah

References

  1. Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA et al. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci U S A 2015; 112:E3574–81 [View Article] [PubMed]
     [Google Scholar]
  2. Lan P, Jiang Y, Zhou J, Yu Y. A global perspective on the convergence of hypervirulence and carbapenem resistance in Klebsiella pneumoniae. J Glob Antimicrob Resist 2021; 25:26–34 [View Article] [PubMed]
     [Google Scholar]
  3. Karampatakis T, Tsergouli K, Behzadi P. Carbapenem-resistant Klebsiella pneumoniae: virulence factors, molecular epidemiology and latest updates in treatment options. Antibiotics 2023; 12:234 [View Article] [PubMed]
     [Google Scholar]
  4. Struve C, Roe CC, Stegger M, Stahlhut SG, Hansen DS et al. Mapping the evolution of hypervirulent Klebsiella pneumoniae. mBio 2015; 6:e00630 [View Article] [PubMed]
     [Google Scholar]
  5. Dai P, Hu D. The making of hypervirulent Klebsiella pneumoniae. J Clin Lab Anal 2022; 36:e24743 [View Article] [PubMed]
     [Google Scholar]
  6. Xie M, Chen K, Ye L, Yang X, Xu Q et al. Conjugation of virulence plasmid in clinical Klebsiella pneumoniae strains through formation of a fusion plasmid. Adv Biosyst 2020; 4:e1900239 [View Article] [PubMed]
     [Google Scholar]
  7. Xu Y, Zhang J, Wang M, Liu M, Liu G et al. Mobilization of the nonconjugative virulence plasmid from hypervirulent Klebsiella pneumoniae. Genome Med 2021; 13:119 [View Article] [PubMed]
     [Google Scholar]
  8. Yang X, Dong N, Chan E-C, Zhang R, Chen S. Carbapenem resistance-encoding and virulence-encoding conjugative plasmids in Klebsiella pneumoniae. Trends Microbiol 2021; 29:65–83 [View Article] [PubMed]
     [Google Scholar]
  9. Wu C, Zhou Y, Ai W, Guo Y, Wu X et al. Co-occurrence of OXA-232, RmtF-encoding plasmids, and pLVPK-like virulence plasmid contributed to the generation of ST15-KL112 hypervirulent multidrug-resistant Klebsiella pneumoniae. Front Microbiol 2023; 14:1133590 [View Article] [PubMed]
     [Google Scholar]
  10. Arcari G, Carattoli A. Global spread and evolutionary convergence of multidrug-resistant and hypervirulent Klebsiella pneumoniae high-risk clones. Pathog Glob Health 2023; 117:328–341 [View Article] [PubMed]
     [Google Scholar]
  11. Turton JF, Payne Z, Coward A, Hopkins KL, Turton JA et al. Virulence genes in isolates of Klebsiella pneumoniae from the UK during 2016, including among carbapenemase gene-positive hypervirulent K1-ST23 and “non-hypervirulent” types ST147, ST15 and ST383. J Med Microbiol 2018; 67:118–128 [View Article] [PubMed]
     [Google Scholar]
  12. Turton J, Davies F, Turton J, Perry C, Payne Z et al. Hybrid resistance and virulence plasmids in “high-risk” clones of Klebsiella pneumoniae, including those carrying blaNDM-5. Microorganisms 2019; 7:326 [View Article]
     [Google Scholar]
  13. Tsui CK-M, Ben Abid F, Al Ismail K, McElheny CL, Al Maslamani M et al. Genomic epidemiology of carbapenem-resistant Klebsiella in Qatar: emergence and dissemination of hypervirulent Klebsiella pneumoniae sequence type 383 Strains. Antimicrob Agents Chemother 2023; 67:e0003023 [View Article] [PubMed]
     [Google Scholar]
  14. Chudejova K, Kraftova L, Mattioni Marchetti V, Hrabak J, Papagiannitsis CC et al. Genetic plurality of OXA/NDM-encoding features characterized from Enterobacterales Recovered From Czech hospitals. Front Microbiol 2021; 12:641415 [View Article] [PubMed]
     [Google Scholar]
  15. Rodrigues C, Desai S, Passet V, Gajjar D, Brisse S. Genomic evolution of the globally disseminated multidrug-resistant Klebsiella pneumoniae clonal group 147. Microb Genom 2022; 8:000737 [View Article] [PubMed]
     [Google Scholar]
  16. Mataseje LF, Chen L, Peirano G, Fakharuddin K, Kreiswith B et al. Klebsiella pneumoniae ST147: and then there were three carbapenemases. Eur J Clin Microbiol Infect Dis 2022; 41:1467–1472 [View Article] [PubMed]
     [Google Scholar]
  17. Tavoschi L, Forni S, Porretta A, Righi L, Pieralli F et al. Prolonged outbreak of New Delhi metallo-beta-lactamase-producing carbapenem-resistant Enterobacterales (NDM-CRE), Tuscany, Italy, 2018 to 2019. Euro Surveill 2020; 25:2000085 [View Article] [PubMed]
     [Google Scholar]
  18. Martin MJ, Corey BW, Sannio F, Hall LR, MacDonald U et al. Anatomy of an extensively drug-resistant Klebsiella pneumoniae outbreak in Tuscany, Italy. Proc Natl Acad Sci U S A 2021; 118:48 [View Article] [PubMed]
     [Google Scholar]
  19. Di Pilato V, Henrici De Angelis L, Aiezza N, Baccani I, Niccolai C et al. Resistome and virulome accretion in an NDM-1-producing ST147 sublineage of Klebsiella pneumoniae associated with an outbreak in Tuscany, Italy: a genotypic and phenotypic characterisation. Lancet Microbe 2022; 3:e224–e234 [View Article] [PubMed]
     [Google Scholar]
  20. Hallal Ferreira Raro O, Nordmann P, Dominguez Pino M, Findlay J, Poirel L. Emergence of carbapenemase-producing hypervirulent Klebsiella pneumoniae in Switzerland. Antimicrob Agents Chemother 2023; 67:e0142422 [View Article] [PubMed]
     [Google Scholar]
  21. Fursova AD, Fursov MV, Astashkin EI, Novikova TS, Fedyukina GN et al. Early response of antimicrobial resistance and virulence genes expression in classical, hypervirulent, and hybrid hvKp-MDR Klebsiella pneumoniae on antimicrobial stress. Antibiotics 2021; 11:7 [View Article] [PubMed]
     [Google Scholar]
  22. Ahmed M, Yang Y, Yang Y, Yan B, Chen G et al. Emergence of hypervirulent carbapenem-resistant Klebsiella pneumoniae coharboring a blaNDM-1-carrying virulent plasmid and a blaKPC-2-carrying plasmid in an Egyptian hospital. mSphere 2021; 6:e00088–21 [View Article]
     [Google Scholar]
  23. Sherif M, Palmieri M, Mirande C, El-Mahallawy H, Rashed HG et al. Whole-genome sequencing of Egyptian multidrug-resistant Klebsiella pneumoniae isolates: a multi-center pilot study. Eur J Clin Microbiol Infect Dis 2021; 40:1451–1460 [View Article] [PubMed]
     [Google Scholar]
  24. Oxford Nanopore Technologies The power of Q20+ chemistry. https://nanoporetech.com/q20plus-chemistry accessed 21 November 2023
  25. Wang J, Bleich RM, Zarmer S, Zhang S, Dogan B et al. Long-read sequencing to interrogate strain-level variation among adherent-invasive Escherichia coli isolated from human intestinal tissue. bioRxiv 2021; 16:e0259141 [View Article] [PubMed]
     [Google Scholar]
  26. Turton JF, Perry C, Claxton A. Do plasmids containing heavy metal resistance genes play a role in neonatal sepsis and invasive disease caused by Klebsiella pneumoniae and Klebsiella variicola?. J Med Microbiol 2022; 71: [View Article] [PubMed]
     [Google Scholar]
  27. Freire B, Ladra S, Parama JR. Memory-efficient assembly using flye. IEEE/ACM Trans Comput Biol Bioinform 2022; 19:3564–3577 [View Article] [PubMed]
     [Google Scholar]
  28. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75:3491–3500 [View Article] [PubMed]
     [Google Scholar]
  29. Carattoli A, Zankari E, Garcia-Fernandez A, Voldby Larsen M, Lund O et al. Plasmidfinder and pMLST: in silico detection and typing of plasmids. Antimicrob Agents Chemother 2014; 58:3895–3903 [View Article]
     [Google Scholar]
  30. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 2012; 50:1355–1361 [View Article] [PubMed]
     [Google Scholar]
  31. Harris SR. SKA: Split Kmer Analysis Toolkit for bacterial genomic epidemiology. Biorxiv 2018 [View Article]
     [Google Scholar]
  32. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15 [View Article] [PubMed]
     [Google Scholar]
  33. Lazareva I, Ageevets V, Sopova J, Lebedeva M, Starkova P et al. The emergence of hypervirulent blaNDM-1-positive Klebsiella pneumoniae sequence type 395 in an oncology hospital. Infect Genet Evol 2020; 85:104527 [View Article] [PubMed]
     [Google Scholar]
  34. Turton JF, Pike R, Perry C, Jenkins C, Turton JA et al. Wide distribution of Escherichia coli carrying IncF plasmids containing blaNDM-5 and rmtB resistance genes from hospitalized patients in England. J Med Microbiol 2022; 71: [View Article] [PubMed]
     [Google Scholar]
  35. Falcone M, Tiseo G, Arcari G, Leonildi A, Giordano C et al. Spread of hypervirulent multidrug-resistant ST147 Klebsiella pneumoniae in patients with severe COVID-19: an observational study from Italy, 2020-21. J Antimicrob Chemother 2022; 77:1140–1145 [View Article] [PubMed]
     [Google Scholar]
  36. Falcone M, Giordano C, Barnini S, Tiseo G, Leonildi A et al. Extremely drug-resistant NDM-9-producing ST147 Klebsiella pneumoniae causing infections in Italy, May 2020. Euro Surveill 2020; 25:48 [View Article] [PubMed]
     [Google Scholar]
  37. Grant JR, Enns E, Marinier E, Mandal A, Herman EK et al. Proksee: in-depth characterization and visualization of bacterial genomes. Nucleic Acids Res 2023; 51:W484–W492 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001823
Loading
Klebsiella pneumoniae sequence type 147: a high-risk clone increasingly associated with plasmids carrying both resistance and virulence elements
J. Med. Microbiol. 73, 001823 (2024); https://doi.org/10.1099/jmm.0.001823
/content/journal/jmm/10.1099/jmm.0.001823
/content/journal/jmm/10.1099/jmm.0.001823
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

Most cited Most Cited RSS feed

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