1887

Abstract

Whole-genome sequencing (WGS) was conducted to characterize -carrying extended-spectrum beta-lactamase (ESBL)-producing (=7). These isolates originated from two pigs (TH2 and TH3) and two humans (TH8 and TH9) from Thailand, and three pigs from Lao PDR (LA1, LA2 and LA3). Four sequence types/serotypes – ST6833/H20 (TH2 and TH3), ST48/O160:H40 (TH8 and TH9), ST5708/H45 (LA1) and ST10562/O148:H30 (LA2 and LA3) – were identified. The plasmid replicon type IncF was identified in all isolates. The point mutations Ser31Thr in PmrA and His2Arg in PmrB were found concurrently in all isolates (colistin MIC=4–8 µg ml). LA1 contained up to five point mutations in PmrB, and the colistin MIC was not significantly different from that for the other isolates. All was located in the IS element, while all was located in the TnIS element. The and genes were co-localized on the same plasmid, which concurrently contained , and . The and genes were located on conjugative plasmids and could be transferred horizontally under selective pressure from ampicillin or colistin. In conclusion, comprehensive insights into the genomic information of ESBL-producing harbouring were obtained. As -carrying ESBL-producing were detected in pigs and humans, a holistic and multisectoral One Health approach is required to contain antimicrobial resistance (AMR).

Funding
This study was supported by the:
  • Royal Golden Jubilee Ph.D. program (Award PHD/0054/2558)
    • Principle Award Recipient: ChanikaPungpian
  • Chulalongkorn University-One Health Research Cluster
    • Principle Award Recipient: RungtipChuanchuen
  • The 90th anniversary of Chulalongkorn University fund (Ratchadaphiseksomphot Endowment Fund)
    • Principle Award Recipient: ChanikaPungpian
  • TRF Basic Research Grant (Award BRG6080014)
    • Principle Award Recipient: RungtipChuanchuen
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001204
2022-06-29
2024-05-04
Loading full text...

Full text loading...

/deliver/fulltext/micro/168/6/mic001204.html?itemId=/content/journal/micro/10.1099/mic.0.001204&mimeType=html&fmt=ahah

References

  1. World Health Organization Critically Important Antimicrobials for Human Medicine, 6th revision. Switzerland: World Health Organization; 2018
  2. Urumova V. Investigations on the resistance of porcine commensal E. coli isolates to beta lactams. Acta Vet Brno 2015; 65:538–547 [View Article]
    [Google Scholar]
  3. Wang Z, Fu Y, Schwarz S, Yin W, Walsh TR et al. Genetic environment of colistin resistance genes mcr-1 and mcr-3 in Escherichia coli from one pig farm in China. Vet Microbiol 2019; 230:56–61 [View Article] [PubMed]
    [Google Scholar]
  4. Zhang P, Wang J, Wang X, Bai X, Ma J et al. Characterization of five Escherichia coli isolates co-expressing ESBL and MCR-1 resistance mechanisms from different origins in China. Front Microbiol 2019; 10:1994 [View Article] [PubMed]
    [Google Scholar]
  5. Liu X, Liu H, Wang L, Peng Q, Li Y et al. Molecular characterization of extended-spectrum β-lactamase-producing multidrug resistant Escherichia coli from swine in northwest China. Front Microbiol 2018; 9:1756 [View Article] [PubMed]
    [Google Scholar]
  6. Carattoli A. Plasmids in Gram negatives: molecular typing of resistance plasmids. Int J Med Microbiol 2011; 301:654–658 [View Article] [PubMed]
    [Google Scholar]
  7. Bai L, Wang L, Yang X, Wang J, Gan X et al. Prevalence and molecular characteristics of extended-spectrum β-lactamase genes in Escherichia coli isolated from diarrheic patients in China. Front Microbiol 2017; 8:144–151 [View Article] [PubMed]
    [Google Scholar]
  8. Seiffert SN, Hilty M, Perreten V, Endimiani A. Extended-spectrum cephalosporin-resistant Gram-negative organisms in livestock: an emerging problem for human health?. Drug Resist Updat 2013; 16:22–45 [View Article] [PubMed]
    [Google Scholar]
  9. Adamski CJ, Cardenas AM, Brown NG, Horton LB, Sankaran B et al. Molecular basis for the catalytic specificity of the CTX-M extended-spectrum β-lactamases. Biochemistry 2015; 54:447–457 [View Article] [PubMed]
    [Google Scholar]
  10. Kim Y-J, Moon J-S, Oh D-H, Chon J-W, Song B-R et al. Genotypic characterization of ESBL-producing E. coli from imported meat in South Korea. Food Res Int 2018; 107:158–164 [View Article] [PubMed]
    [Google Scholar]
  11. Xu G, An W, Wang H, Zhang X. Prevalence and characteristics of extended-spectrum β-lactamase genes in Escherichia coli isolated from piglets with post-weaning diarrhea in Heilongjiang province, China. Front Microbiol 2015; 6:1103–1011 [View Article]
    [Google Scholar]
  12. Lay KK, Jeamsripong S, Sunn KP, Angkititrakul S, Prathan R et al. Colistin resistance and ESBL production in Salmonella and Escherichia coli from pigs and pork in the Thailand, Cambodia, Lao PDR, and Myanmar Border Area. Antibiotics (Basel) 2021; 10:657 [View Article]
    [Google Scholar]
  13. Liu Y-Y, Wang Y, Walsh TR, Yi L-X, Zhang R et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 2016; 16:161–168 [View Article]
    [Google Scholar]
  14. Xavier BB, Lammens C, Ruhal R, Kumar-Singh S, Butaye P et al. Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016. Euro Surveill 2016; 21:30280 [View Article]
    [Google Scholar]
  15. AbuOun M, Stubberfield EJ, Duggett NA, Kirchner M, Dormer L et al. mcr-1 and mcr-2 variant genes identified in Moraxella species isolated from pigs in Great Britain from 2014 to 2015. J Antimicrob Chemother 2017; 72:2745–2749 [View Article]
    [Google Scholar]
  16. Borowiak M, Fischer J, Hammerl JA, Hendriksen RS, Szabo I et al. Identification of a novel transposon-associated phosphoethanolamine transferase gene, mcr-5, conferring colistin resistance in d-tartrate fermenting Salmonella enterica subsp. enterica serovar Paratyphi B. J Antimicrob Chemother 2017; 72:3317–3324 [View Article] [PubMed]
    [Google Scholar]
  17. 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. Euro Surveill 2017; 22:30589 [View Article] [PubMed]
    [Google Scholar]
  18. Yin W, Li H, Shen Y, Liu Z, Wang S et al. Novel plasmidmediated colistin resistance gene mcr-3 in Escherichia coli. mBio 2017; 8:e00543–17 [View Article]
    [Google Scholar]
  19. Wang X, Wang Y, Zhou Y, Li J, Yin W et al. Emergence of a novel mobile colistin resistance gene, mcr-8, in NDM-producing Klebsiella pneumoniae. Emerg Microbes Infect 2018; 7:122 [View Article] [PubMed]
    [Google Scholar]
  20. Yang YQ, Li YX, Lei CW, Zhang AY, Wang HN. Novel plasmid-mediated colistin resistance gene mcr-7.1 in Klebsiella pneumoniae. J Antimicrob Chemother 2018; 73:1791–1795 [View Article] [PubMed]
    [Google Scholar]
  21. Carroll LM, Gaballa A, Guldimann C, Sullivan G, Henderson LO et al. Identification of novel mobilized colistin resistance gene mcr-9 in a multidrug-resistant, colistin-susceptible Salmonella enterica Serotype Typhimurium isolate. mBio 2019; 10:e00853-19 [View Article] [PubMed]
    [Google Scholar]
  22. Wang C, Feng Y, Liu L, Wei L, Kang M et al. Identification of novel mobile colistin resistance gene mcr-10. Emerg Microbes Infect 2020; 9:508–516 [View Article] [PubMed]
    [Google Scholar]
  23. Orlek A, Stoesser N, Anjum MF, Doumith M, Ellington MJ et al. Plasmid classification in an era of whole-genome sequencing: application in studies of antibiotic resistance epidemiology. Front Microbiol 2017; 8:182 [View Article] [PubMed]
    [Google Scholar]
  24. Eiamphungporn W, Yainoy S, Jumderm C, Tan-Arsuwongkul R, Tiengrim S et al. Prevalence of the colistin resistance gene mcr-1 in colistin-resistant Escherichia coli and Klebsiella pneumoniae isolated from humans in Thailand. J Glob Antimicrob Resist 2018; 15:32–35 [View Article] [PubMed]
    [Google Scholar]
  25. Khine NO, Lugsomya K, Kaewgun B, Honhanrob L, Pairojrit P et al. Multidrug resistance and virulence factors of Escherichia coli harboring plasmid-mediated colistin resistance: mcr-1 and mcr-3 genes in contracted pig farms in Thailand. Front Vet Sci 2020; 7:582899 [PubMed]
    [Google Scholar]
  26. Pungpian C, Sinwat N, Angkititrakul S, Prathan R, Chuanchuen R. Presence and transfer of antimicrobial resistance determinants in Escherichia coli in pigs, pork, and humans in Thailand and lao PDR border province. Microb Drug Resist 2021; 27:571–584 [PubMed]
    [Google Scholar]
  27. Batchelor M, Hopkins K, Threlfall EJ, Clifton-Hadley FA, Stallwood AD et al. bla(CTX-M) genes in clinical Salmonella isolates recovered from humans in England and Wales from 1992 to 2003. Antimicrob Agents Chemother 2005; 49:1319–1322 [View Article] [PubMed]
    [Google Scholar]
  28. Hasman H, Mevius D, Veldman K, Olesen I, Aarestrup FM. beta-Lactamases among extended-spectrum beta-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. J Antimicrob Chemother 2005; 56:115–121 [View Article] [PubMed]
    [Google Scholar]
  29. Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Disk and Dilution Susceptibility test for Bacteria Isolated From Animals 3rd VET01-S3 Wayne, PA: Clinical and Laboratory Standards Institute; 2015
    [Google Scholar]
  30. EUCAST The European Committee on Antimicrobial Susceptibility Testing: Break point Tables for Interpretation of MICs; 2018 http://www.eucast.org
  31. Rebelo AR, Bortolaia V, Kjeldgaard JS, Pedersen SK, Leekitcharoenphon P et al. Multiplex PCR for detection of plasmid-mediated colistin resistance determinants, mcr-1, mcr-2, mcr-3, mcr-4 and mcr-5 for surveillance purposes. Euro Surveill 2018; 23: [View Article]
    [Google Scholar]
  32. Khemtong S, Chuanchuen R. Class 1 integrons and Salmonella genomic island 1 among Salmonella enterica isolated from poultry and swine. Microb Drug Resist 2008; 14:65–70 [View Article] [PubMed]
    [Google Scholar]
  33. Yamaguchi T, Kawahara R, Harada K, Teruya S, Nakayama T et al. The presence of colistin resistance gene mcr-1 and -3 in ESBL producing Escherichia coli isolated from food in Ho Chi Minh City, Vietnam. FEMS Microbiol Lett 2018; 365:1–8 [View Article]
    [Google Scholar]
  34. Andrews S. FastQC: a quality control tool for high throughput sequence data; 2010 http://www.bioinformatics.babraham.ac.uk/projects/fastqc
  35. 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] [PubMed]
    [Google Scholar]
  36. 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]
  37. Joensen KG, Tetzschner AMM, Iguchi A, Aarestrup FM, Scheutz F. Rapid and easy in silico serotyping of Escherichia coli isolates by use of whole-genome sequencing data. J Clin Microbiol 2015; 53:2410–2426 [View Article] [PubMed]
    [Google Scholar]
  38. 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]
  39. Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS et al. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol 2014; 52:1501–1510 [View Article] [PubMed]
    [Google Scholar]
  40. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014; 58:3895–3903 [View Article] [PubMed]
    [Google Scholar]
  41. Flament-Simon S-C, de Toro M, Mora A, García V, García-Meniño I et al. Whole genome sequencing and characteristics of mcr-1-Harboring plasmids of porcine Escherichia coli isolates belonging to the high-risk clone O25b:H4-ST131 clade B. Front Microbiol 2020; 11:387 [View Article] [PubMed]
    [Google Scholar]
  42. Touati M, Hadjadj L, Berrazeg M, Baron SA, Rolain JM. Emergence of Escherichia coli harbouring mcr-1 and mcr-3 genes in North West Algerian farmlands. J Glob Antimicrob Resist 2020; 21:132–137 [View Article] [PubMed]
    [Google Scholar]
  43. Sato T, Shiraishi T, Hiyama Y, Honda H, Shinagawa M et al. Contribution of novel amino acid alterations in PmrA or PmrB to colistin resistance in mcr-negative Escherichia coli clinical isolates, including major multidrug-resistant lineages O25b:H4-ST131-H30Rx and Non-x. Antimicrob Agents Chemother 2018; 62:e00864-18 [View Article] [PubMed]
    [Google Scholar]
  44. Luo Q, Niu T, Wang Y, Yin J, Wan F et al. In vitro reduction of colistin susceptibility and comparative genomics reveals multiple differences between MCR-positive and MCR-negative colistin-resistant Escherichia coli. Infect Drug Resist 2019; 12:1665–1674 [View Article] [PubMed]
    [Google Scholar]
  45. Poirel L, Kieffer N, Nordmann P. In vitro study of isapl1-mediated mobilization of the colistin resistance gene mcr-1. Antimicrob Agents Chemother 2017; 61: [View Article]
    [Google Scholar]
  46. Snesrud E, McGann P, Chandler M. The birth and demise of the isapl1-mcr-1-isapl1 composite transposon: the vehicle for transferable colistin resistance. MBio 2018; 9: [View Article]
    [Google Scholar]
  47. Li R, Du P, Zhang P, Li Y, Yang X et al. Comprehensive genomic investigation of coevolution of mcr genes in Escherichia coli strains via nanopore sequencing. Glob Chall 2021; 5:2000014 [View Article] [PubMed]
    [Google Scholar]
  48. Wang Z, Fu Y, Du XD, Jiang H, Wang Y. Potential transferability of mcr-3 via IS26-mediated homologous recombination in Escherichia coli. Emerg Microbes Infect 2018; 7:55 [View Article] [PubMed]
    [Google Scholar]
  49. Hadjadj L, Baron SA, Olaitan AO, Morand S, Rolain JM. Co-occurrence of variants of mcr-3 and mcr-8 genes in a Klebsiella pneumoniae isolate from Laos. Front Microbiol 2019; 10: [View Article]
    [Google Scholar]
  50. Liu L, Feng Y, Zhang XX, McNally A, Zong ZY. New variant of mcr-3 in an extensively drug-resistant Escherichia coli clinical isolate carrying mcr-1 and bla(NDM-5). Antimicrob Agents Chemother 2017; 61: [View Article]
    [Google Scholar]
  51. Long H, Feng Y, Ma K, Liu L, McNally A et al. The co-transfer of plasmid-borne colistin-resistant genes mcr-1 and mcr-3.5, the carbapenemase gene blaNDM-5 and the 16S methylase gene rmtB from Escherichia coli. Sci Rep 2019; 9:696 [View Article]
    [Google Scholar]
  52. Sun J, Li X-P, Fang L-X, Sun R-Y, He Y-Z et al. Co-occurrence of mcr-1 in the chromosome and on an IncHI2 plasmid: persistence of colistin resistance in Escherichia coli. Int J Antimicrob Agents 2018; 51:842–847 [View Article]
    [Google Scholar]
  53. Shen C, Zhong L-L, Ma F, El-Sayed Ahmed MAE-G, Doi Y et al. Genomic patterns and characterizations of chromosomally-encoded mcr-1 in Escherichia coli populations. Gut Pathog 2020; 12:55 [View Article]
    [Google Scholar]
  54. García-Meniño I, Díaz-Jiménez D, García V, de Toro M, Flament-Simon SC et al. Genomic characterization of prevalent mcr-1, mcr-4, and mcr-5 Escherichia coli within swine enteric colibacillosis in Spain. Front Microbiol 2019; 10: [View Article]
    [Google Scholar]
  55. van Duijkeren E, Schink A-K, Roberts MC, Wang Y, Schwarz S. Mechanisms of bacterial resistance to antimicrobial agents. Microbiol Spectr 2018; 6:51–82 [View Article]
    [Google Scholar]
  56. Travis RM, Gyles CL, Reid-Smith R, Poppe C, McEwen SA et al. Chloramphenicol and kanamycin resistance among porcine Escherichia coli in Ontario. J Antimicrob Chemother 2006; 58:173–177 [View Article] [PubMed]
    [Google Scholar]
  57. Shropshire WC, Aitken SL, Pifer R, Kim J, Bhatti MM et al. IS26-mediated amplification of blaOXA-1 and blaCTX-M-15 with concurrent outer membrane porin disruption associated with de novo carbapenem resistance in a recurrent bacteraemia cohort. J Antimicrob Chemother 2021; 76:385–395 [View Article] [PubMed]
    [Google Scholar]
  58. Capitani G, De Biase D, Aurizi C, Gut H, Bossa F et al. Crystal structure and functional analysis of Escherichia coli glutamate decarboxylase. EMBO J 2003; 22:4027–4037 [View Article] [PubMed]
    [Google Scholar]
  59. Anantharaman V, Iyer LM, Aravind L. Ter-dependent stress response systems: novel pathways related to metal sensing, production of a nucleoside-like metabolite, and DNA-processing. Mol Biosyst 2012; 8:3142–3165 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001204
Loading
/content/journal/micro/10.1099/mic.0.001204
Loading

Data & Media loading...

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