1887

Abstract

is a ubiquitous bacterium that has been widely exposed to antibiotics over the last 70 years. It has adapted by acquiring different antibiotic-resistance genes (ARGs), the census of which we aim to characterize here. To do so, we analysed 70 301 genomes obtained from the EnteroBase database and detected 1 027 651 ARGs using the AMRFinder, Mustard and ResfinderFG ARG databases. We observed a strong phylogroup and clonal lineage specific distribution of some ARGs, supporting the argument for epistasis between ARGs and the strain genetic background. However, each phylogroup had ARGs conferring a similar antibiotic class resistance pattern, indicating phenotypic adaptive convergence. The G+C content or the type of ARG was not associated with the frequency of the ARG in the database. In addition, we identified ARGs from anaerobic, non- bacteria in four genomes of , supporting the hypothesis that the transfer between anaerobic bacteria and can spontaneously occur but remains exceptional. In conclusion, we showed that phylum barrier and intra-species phylogenetic history are major drivers of the acquisition of a resistome in .

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000489
2021-08-26
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/mgen/7/8/mgen000489.html?itemId=/content/journal/mgen/10.1099/mgen.0.000489&mimeType=html&fmt=ahah

References

  1. Slanetz LW, Bartley CH. Numbers of enterococci in water, sewage, and feces determined by the membrane filter technique with an improved medium. J Bacteriol 1957; 74:591–595 [View Article] [PubMed]
    [Google Scholar]
  2. Tenaillon O, Skurnik D, Picard B, Denamur E. The population genetics of commensal Escherichia coli. Nat Rev Microbiol 2010; 8:207–217 [View Article] [PubMed]
    [Google Scholar]
  3. Smati M, Clermont O, Bleibtreu A, Fourreau F, David A et al. Quantitative analysis of commensal Escherichia coli populations reveals host-specific enterotypes at the intra-species level. Microbiologyopen 2015; 4:604–615 [View Article] [PubMed]
    [Google Scholar]
  4. Skurnik D, Ruimy R, Andremont A, Amorin C, Rouquet P et al. Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli. J Antimicrob Chemother 2006; 57:1215–1219 [View Article] [PubMed]
    [Google Scholar]
  5. Liu B, Pop M. ARDB – antibiotic resistance genes database. Nucleic Acids Res 2009; 37:D443–D447 [View Article]
    [Google Scholar]
  6. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 2012; 67:2640–2644 [View Article] [PubMed]
    [Google Scholar]
  7. Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res 2017; 45:D566–D573 [View Article]
    [Google Scholar]
  8. Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M et al. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 2014; 58:212–220 [View Article] [PubMed]
    [Google Scholar]
  9. Feldgarden M, Brover V, Haft DH, Prasad AB, Slotta DJ et al. Using the NCBI AMRFinder tool to determine antimicrobial resistance genotype-phenotype correlations within a collection of narms isolates. bioRxiv 2019550707
    [Google Scholar]
  10. Sommer MOA, Dantas G, Church GM. Functional characterization of the antibiotic resistance reservoir in the human microflora. Science 2009; 325:1128–1131 [View Article] [PubMed]
    [Google Scholar]
  11. Ruppé E, Ghozlane A, Tap J, Pons N, Alvarez AS et al. Prediction of the intestinal resistome by a three-dimensional structure-based method. Nat Microbiol 2019; 4:112–123 [View Article] [PubMed]
    [Google Scholar]
  12. Wallace JC, Port JA, Smith MN, Faustman EM. FARME DB: a functional antibiotic resistance element database. Database 2017; 2017:baw165 [View Article]
    [Google Scholar]
  13. Munk P, Knudsen BE, Lukjancenko O, Duarte ASR, Van Gompel L et al. Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries. Nat Microbiol 2018; 3:898–908 [View Article] [PubMed]
    [Google Scholar]
  14. Ebmeyer S, Kristiansson E, Larsson DGJ. A framework for identifying the recent origins of mobile antibiotic resistance genes. Commun Biol 2021; 4:8 [View Article]
    [Google Scholar]
  15. Deng M, Zhu M-H, Li J-J, Bi S, Sheng Z-K et al. Molecular epidemiology and mechanisms of tigecycline resistance in clinical isolates of Acinetobacter baumannii from a Chinese university hospital. Antimicrob Agents Chemother 2014; 58:297–303 [View Article]
    [Google Scholar]
  16. Stalder T, Barraud O, Casellas M, Dagot C, Ploy MC. Integron involvement in environmental spread of antibiotic resistance. Front Microbiol 2012; 3:119 [View Article] [PubMed]
    [Google Scholar]
  17. Branger C, Ledda A, Billard-Pomares T, Doublet B, Barbe V et al. Specialization of small non-conjugative plasmids in Escherichia coli according to their family types. Microb Genom 2019; 5:000281 [View Article] [PubMed]
    [Google Scholar]
  18. Branger C, Ledda A, Billard-Pomares T, Doublet B, Fouteau S et al. Extended-spectrum β-lactamase-encoding genes are spreading on a wide range of Escherichia coli plasmids existing prior to the use of third-generation cephalosporins. Microb Genom 2018; 4:000203 [View Article] [PubMed]
    [Google Scholar]
  19. Billard-Pomares T, Fouteau S, Jacquet ME, Roche D, Barbe V et al. Characterization of a P1-like bacteriophage carrying an SHV-2 extended-spectrum β-lactamase from an Escherichia coli strain. Antimicrob Agents Chemother 2014; 58:6550–6557 [View Article] [PubMed]
    [Google Scholar]
  20. Branger C, Zamfir O, Geoffroy S, Laurans G, Arlet G et al. Genetic background of Escherichia coli and extended-spectrum beta-lactamase type. Emerg Infect Dis 2005; 11:54–61 [View Article] [PubMed]
    [Google Scholar]
  21. Deschamps C, Clermont O, Hipeaux MC, Arlet G, Denamur E et al. Multiple acquisitions of CTX-M plasmids in the rare D2 genotype of Escherichia coli provide evidence for convergent evolution. Microbiology 2009; 155:1656–1668 [View Article] [PubMed]
    [Google Scholar]
  22. Johnson JR, Goullet P, Picard B, Moseley SL, Roberts PL et al. Association of carboxylesterase B electrophoretic pattern with presence and expression of urovirulence factor determinants and antimicrobial resistance among strains of Escherichia coli that cause urosepsis. Infect Immun 1991; 59:2311–2315 [View Article] [PubMed]
    [Google Scholar]
  23. Johnson JR, Orskov I, Orskov F, Goullet P, Picard B et al. O, K, and H antigens predict virulence factors, carboxylesterase B pattern, antimicrobial resistance, and host compromise among Escherichia coli strains causing urosepsis. J Infect Dis 1994; 169:119–126 [View Article] [PubMed]
    [Google Scholar]
  24. Horesh G, Blackwell GA, Tonkin-Hill G, Corander J, Heinz E et al. A comprehensive and high-quality collection of Escherichia coli genomes and their genes. Microb Genom 2021; 7:000499 [View Article]
    [Google Scholar]
  25. Touchon M, Perrin A, de Sousa JAM, Vangchhia B, Burn S et al. Phylogenetic background and habitat drive the genetic diversification of Escherichia coli. . PLoS Genet 2020; 16:e1008866 [View Article] [PubMed]
    [Google Scholar]
  26. Manges AR, Johnson JR, Foxman B, O’Bryan TT, Fullerton KE et al. Widespread distribution of urinary tract infections caused by a multidrug-resistant Escherichia coli clonal group. N Engl J Med 2001; 345:1007–1013 [View Article] [PubMed]
    [Google Scholar]
  27. 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]
  28. Kondratyeva K, Salmon-Divon M, Navon-Venezia S. Meta-analysis of pandemic Escherichia coli ST131 plasmidome proves restricted plasmid-clade associations. Sci Rep 2020; 10:36 [View Article] [PubMed]
    [Google Scholar]
  29. Domingo J, Baeza-Centurion P, Lehner B. The causes and consequences of genetic interactions (epistasis. Annu Rev Genomics Hum Genet 2019; 20:433–460 [View Article] [PubMed]
    [Google Scholar]
  30. Zhou Z, Alikhan N-F, Mohamed K, Fan Y. Agama Study Group et al. The EnteroBase user’s guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity. Genome Res 2020; 30:138–152 [View Article]
    [Google Scholar]
  31. Sahl JW, Morris CR, Emberger J, Fraser CM, Ochieng JB et al. Defining the phylogenomics of Shigella species: a pathway to diagnostics. J Clin Microbiol 2015; 53:951–960 [View Article] [PubMed]
    [Google Scholar]
  32. Beghain J, Bridier-Nahmias A, Le Nagard H, Denamur E, Clermont O. ClermonTyping: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping. Microb Genom 2018; 4:000192 [View Article] [PubMed]
    [Google Scholar]
  33. Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 2016; 17:132 [View Article] [PubMed]
    [Google Scholar]
  34. Clermont O, Dixit OVA, Vangchhia B, Condamine B, Dion S et al. Characterization and rapid identification of phylogroup G in Escherichia coli, a lineage with high virulence and antibiotic resistance potential. Environ Microbiol 2019; 21:3107–3117 [View Article] [PubMed]
    [Google Scholar]
  35. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods 2015; 12:59–60 [View Article] [PubMed]
    [Google Scholar]
  36. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol 2019; 20:257 [View Article] [PubMed]
    [Google Scholar]
  37. Carattoli A, Zankari E, García-Fernández A, Larsen MV, 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
    [Google Scholar]
  38. Jolley KA, Maiden MC. BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 2010; 11:595 [View Article] [PubMed]
    [Google Scholar]
  39. Bohlin J, Eldholm V, Pettersson JHO, Brynildsrud O, Snipen L. The nucleotide composition of microbial genomes indicates differential patterns of selection on core and accessory genomes. BMC Genomics 2017; 18:151 [View Article] [PubMed]
    [Google Scholar]
  40. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 2012; 28:3150–3152 [View Article] [PubMed]
    [Google Scholar]
  41. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006; 22:1658–1659 [View Article] [PubMed]
    [Google Scholar]
  42. Kim S-W, Karns JS, Van Kessel JS, Haley BJ. Genome sequences of 30 Escherichia coli O157:H7 isolates recovered from a single dairy farm and its associated off-site heifer-raising facility. Genome Announc 2017; 5:e00814-17
    [Google Scholar]
  43. Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V et al. The complete genome sequence of Escherichia coli K-12. Science 1997; 277:1453–1462 [View Article] [PubMed]
    [Google Scholar]
  44. Porse A, Schou TS, Munck C, Ellabaan MMH, Sommer MOA. Biochemical mechanisms determine the functional compatibility of heterologous genes. Nat Commun 2018; 9:522 [View Article] [PubMed]
    [Google Scholar]
  45. Mellmann A, Bletz S, Böking T, Kipp F, Becker K et al. Real-time genome sequencing of resistant bacteria provides precision infection control in an institutional setting. J Clin Microbiol 2016; 54:2874–2881 [View Article] [PubMed]
    [Google Scholar]
  46. Jain R, Rivera MC, Lake JA. Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci USA 1999; 96:3801–3806 [View Article] [PubMed]
    [Google Scholar]
  47. Denamur E, Clermont O, Bonacorsi S, Gordon D. The population genetics of pathogenic Escherichia coli. Nat Rev Microbiol 2021; 19:37–54 [View Article] [PubMed]
    [Google Scholar]
  48. Escobar-Páramo P, Clermont O, Blanc-Potard AB, Bui H, Le Bouguénec C et al. A specific genetic background is required for acquisition and expression of virulence factors in Escherichia coli. Mol Biol Evol 2004; 21:1085–1094 [View Article] [PubMed]
    [Google Scholar]
  49. Card KJ, Thomas MD, Graves JL, Barrick JE, Lenski RE. Genomic evolution of antibiotic resistance is contingent on genetic background following a long-term experiment with Escherichia coli. Proc Natl Acad Sci USA 2021; 118:e2016886118 [View Article] [PubMed]
    [Google Scholar]
  50. Leski TA, Bangura U, Jimmy DH, Ansumana R, Lizewski SE et al. Multidrug-resistant tet(X)-containing hospital isolates in Sierra Leone. Int J Antimicrob Agents 2013; 42:83–86 [View Article] [PubMed]
    [Google Scholar]
  51. Li J, Jia H, Cai X, Zhong H, Feng Q et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol 2014; 32:834–841 [View Article] [PubMed]
    [Google Scholar]
  52. Bonnet R. Growing group of extended-spectrum beta-lactamases: the CTX-M enzymes. Antimicrob Agents Chemother 2004; 48:1–14 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000489
Loading
/content/journal/mgen/10.1099/mgen.0.000489
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
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