-like genome architecture among carbapenemase-producing and in the Netherlands Open Access

Abstract

Carbapenem-hydrolysing enzymes belonging to the OXA-48-like group are encoded by -like alleles and are abundant among in the Netherlands. Therefore, the objective here was to investigate the characteristics, gene content and diversity of the -like carrying plasmids and chromosomes of and collected in the Dutch national surveillance from 2014 to 2019 in comparison with genome sequences from 29 countries. A combination of short-read genome sequencing with long-read sequencing enabled the reconstruction of 47 and 132 complete -like plasmids for and , respectively. Seven distinct plasmid groups designated as pOXA-48-1 to pOXA-48-5, pOXA-181 and pOXA-232 were identified in the Netherlands which were similar to internationally reported plasmids obtained from countries from North and South America, Europe, Asia and Oceania. The seven plasmid groups varied in size, G+C content, presence of antibiotic resistance genes, replicon family and gene content. The pOXA-48-1 to pOXA-48-5 plasmids were variable, and the pOXA-181 and pOXA-232 plasmids were conserved. The pOXA-48-1, pOXA-48-2, pOXA-48-3 and pOXA-48-5 groups contained a putative conjugation system, but this was absent in the pOXA-48-4, pOXA-181 and pOXA-232 plasmid groups. pOXA-48 plasmids contained the PemI antitoxin, while the pOXA-181 and pOXA-232 plasmids did not. Furthermore, the pOXA-181 plasmids carried a type IV secretion system, while the pOXA-48 plasmids and pOXA-232 lacked this system. A group of non-related pOXA-48 plasmids from the Netherlands contained different resistance genes, non-IncL-type replicons or no replicons. Whole genome multilocus sequence typing revealed that the -like plasmids were found in a wide variety of genetic backgrounds in contrast to chromosomally encoded -like alleles. Chromosomally localized and alleles were located on genetic elements of variable sizes and comprised regions of pOXA-48 plasmids. The -like genetic element was flanked by a direct repeat upstream of IS1R, and was found at multiple locations in the chromosomes of . Lastly, isolates carrying or were mostly resistant for meropenem, whereas , and chromosomal or isolates were mostly sensitive. In conclusion, the overall -like plasmid population in the Netherlands is conserved and similar to that reported for other countries, confirming global dissemination of -like plasmids. Variations in size, presence of antibiotic resistance genes and gene content impacted pOXA-48, pOXA-181 and pOXA-232 plasmid architecture.

Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000512
2021-05-07
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/mgen/7/5/mgen000512.html?itemId=/content/journal/mgen/10.1099/mgen.0.000512&mimeType=html&fmt=ahah

References

  1. Logan LK, Weinstein RA. The epidemiology of carbapenem-resistant Enterobacteriaceae: the impact and evolution of a global menace. J Infect Dis 2017; 215:S28–S36 [View Article]
    [Google Scholar]
  2. Kopotsa K, Osei Sekyere J, Mbelle NM. Plasmid evolution in carbapenemase-producing Enterobacteriaceae: a review. Ann N Y Acad Sci 2019
    [Google Scholar]
  3. Hendrickx APA, Landman F, de Haan A, Borst D, Witteveen S et al. Plasmid diversity among genetically related Klebsiella pneumoniae bla KPC-2 and bla KPC-3 isolates collected in the Dutch national surveillance. Sci Rep 2020; 10:16778
    [Google Scholar]
  4. van der Zwaluw K, Witteveen S, Wielders L, van Santen M, Landman F et al. Molecular characteristics of carbapenemase-producing Enterobacterales in the Netherlands; results of the 2014-2018 national laboratory surveillance. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis 2020
    [Google Scholar]
  5. Ambler RP, Coulson AF, Frère JM, Ghuysen JM, Joris B et al. A standard numbering scheme for the class A beta-lactamases. Biochem J 1991; 276:269–270
    [Google Scholar]
  6. Pitout JDD, Peirano G, Kock MM, Strydom K-A, Matsumura Y. The global ascendency of OXA-48-Type carbapenemases. Clin Microbiol Rev 18 2019; 33:
    [Google Scholar]
  7. Oueslati S, Nordmann P, Poirel L. Heterogeneous hydrolytic features for OXA-48-like β-lactamases. J Antimicrob Chemother 2015; 70:1059–1063
    [Google Scholar]
  8. Poirel L, Héritier C, Tolün V, Nordmann P. Emergence of oxacillinase-mediated resistance to imipenem in Klebsiella pneumoniae. Antimicrob Agents Chemother 2004; 48:15–22 [View Article]
    [Google Scholar]
  9. Potron A, Nordmann P, Lafeuille E, Al Maskari Z, Al Rashdi F et al. Characterization of OXA-181, a carbapenem-hydrolyzing class D β-lactamase from Klebsiella pneumoniae. Antimicrob Agents Chemother 2011; 55:4896–4899 [View Article]
    [Google Scholar]
  10. Potron A, Rondinaud E, Poirel L, Belmonte O, Boyer S et al. Genetic and biochemical characterisation of OXA-232, a carbapenem-hydrolysing class D β-lactamase from Enterobacteriaceae. Int J Antimicrob Agents 2013; 41:325–329 [View Article]
    [Google Scholar]
  11. Oteo J, Hernández JM, Espasa M, Fleites A, Sáez D et al. Emergence of OXA-48-producing Klebsiella pneumoniae and the novel carbapenemases OXA-244 and OXA-245 in Spain. J of Antimicrobial Chemother 2013; 68:317–321 [View Article]
    [Google Scholar]
  12. Carattoli A. Resistance plasmid families in Enterobacteriaceae. Antimicrob Agents Chemother 2009; 53:2227–2238 [View Article]
    [Google Scholar]
  13. Carattoli A, Seiffert SN, Schwendener S, Perreten V, Endimiani A. Differentiation of IncL and IncM plasmids associated with the spread of clinically relevant antimicrobial resistance. PLoS One 2015; 10:e0123063 [View Article]
    [Google Scholar]
  14. Poirel L, Bonnin RA, Nordmann P. Genetic features of the widespread plasmid coding for the carbapenemase OXA-48. Antimicrob Agents Chemother 2012; 56:559–562 [View Article]
    [Google Scholar]
  15. Beyrouthy R, Robin F, Delmas J, Gibold L, Dalmasso G et al. IS 1R -mediated plasticity of IncL/M plasmids leads to the insertion of bla OXA-48 into the Escherichia coli chromosome. Antimicrob Agents Chemother 2014; 58:3785–3790 [View Article]
    [Google Scholar]
  16. Potron A, Poirel L, Nordmann P. Origin of OXA-181, an emerging carbapenem-hydrolyzing oxacillinase, as a chromosomal gene in Shewanella xiamenensis. Antimicrob Agents Chemother 2011; 55:4405–4407 [View Article]
    [Google Scholar]
  17. Liu Y, Feng Y, Wu W, Xie Y, Wang X et al. First report of OXA-181-producing Escherichia coli in China and characterization of the isolate using whole-genome sequencing. Antimicrob Agents Chemother 2015; 59:5022–5025 [View Article]
    [Google Scholar]
  18. Turton JF, Doumith M, Hopkins KL, Perry C, Meunier D et al. Clonal expansion of Escherichia coli ST38 carrying a chromosomally integrated OXA-48 carbapenemase gene. J Med Microbiol 2016; 65:538–546 [View Article]
    [Google Scholar]
  19. Mataseje LF, Boyd DA, Fuller J, Haldane D, Hoang L et al. Characterization of OXA-48-like carbapenemase producers in Canada, 2011–14. J Antimicrob Chemother 2018; 73:626–633 [View Article]
    [Google Scholar]
  20. van der Zwaluw K, de Haan A, Pluister GN, Bootsma HJ, de Neeling AJ et al. The carbapenem inactivation method (CIM), a simple and low-cost alternative for the Carba NP test to assess phenotypic carbapenemase activity in gram-negative rods. PLoS One 2015; 10:e0123690 [View Article]
    [Google Scholar]
  21. Carattoli A, Villa L, Feudi C, Curcio L, Orsini S et al. Novel plasmid-mediated colistin resistance mcr-4 gene in Salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016. Eurosurveillance 2017; 22:30589 [View Article]
    [Google Scholar]
  22. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S et al. Identification of acquired antimicrobial resistance genes. Journal of Antimicrobial Chemotherapy 2012; 67:2640–2644 [View Article]
    [Google Scholar]
  23. Loman NJ, Quinlan AR. Poretools: a toolkit for analyzing nanopore sequence data. Bioinformatics 2014; 30:3399–3401 [View Article]
    [Google Scholar]
  24. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article]
    [Google Scholar]
  25. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
    [Google Scholar]
  26. Köster J, Rahmann S. Snakemake-a scalable bioinformatics workflow engine. Bioinformatics 2018; 34:3600 [View Article][PubMed]
    [Google Scholar]
  27. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article]
    [Google Scholar]
  28. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [View Article]
    [Google Scholar]
  29. Boutet E, Lieberherr D, Tognolli M, Schneider M, Bairoch A. UniProtKB/Swiss-Prot. Methods Mol Biol Clifton NJ 2007; 406:89–112
    [Google Scholar]
  30. Palmieri M, D’Andrea MM, Pelegrin AC, Mirande C, Brkic S et al. Genomic epidemiology of carbapenem- and colistin-resistant Klebsiella pneumoniae isolates from serbia: predominance of ST101 strains carrying a novel OXA-48 plasmid. Front Microbiol 2020; 11:294 [View Article]
    [Google Scholar]
  31. Jousset AB, Dabos L, Bonnin RA, Girlich D, Potron A. Ctx-M-15-producing Shewanella species clinical isolate expressing OXA-535, a Chromosome-Encoded OXA-48 variant, putative progenitor of the plasmid-encoded OXA-436. Antimicrob Agents Chemother 2018 https://aac.asm.org/content/62/1/e01879-17
    [Google Scholar]
  32. Moussa J, Panossian B, Nassour E, Salloum T, Abboud E et al. Detailed characterization of an IncFII plasmid carrying blaOXA-48 from Lebanon. J Antimicrob Chemother 2020; 75:2462–2465 [View Article]
    [Google Scholar]
  33. Rojas LJ, Hujer AM, Rudin SD, Wright MS, Domitrovic TN et al. NDM-5 and OXA-181 beta-lactamases, a significant threat continues to spread in the Americas. Antimicrob Agents Chemother 2017; 61: [View Article]
    [Google Scholar]
  34. Shen Z, Zhang H, Gao Q, Qin J, Zhang C et al. Increased plasmid copy number contributes to the elevated carbapenem resistance in OXA-232-producing Klebsiella pneumoniae. Microb Drug Resist 2020; 26:561–568 [View Article][PubMed]
    [Google Scholar]
  35. Sugawara E, Kojima S, Nikaido H. Klebsiella pneumoniae major porins OmpK35 and OmpK36 allow more efficient diffusion of β-Lactams than their Escherichia coli homologs OmpF and OmpC. J Bacteriol 2016; 198:3200–3208 [View Article]
    [Google Scholar]
  36. Davin-Regli A, Bolla J-M, James C, Lavigne J-P, Chevalier J et al. Membrane permeability and regulation of drug ‘influx and efflux’ in enterobacterial pathogens. Curr Drug Targets. september 2008; 9:750–759 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000512
Loading
/content/journal/mgen/10.1099/mgen.0.000512
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

Most cited Most Cited RSS feed