1887

Abstract

The presence of antibiotic-resistance (AR) genes in foodborne bacteria of enteric origin represents a relevant threat to human health in the case of opportunistic pathogens, which can reach the human gut through the food chain. is a human opportunistic pathogen often associated with infections in immune-compromised or cancer patients, and it can also be detected in the environment, including fermented foods. We have focused on the molecular characterization of a tetracycline (Tet)-resistance gene present in 39 foodborne isolates of phenotypically resistant to this drug. The gene was identified as a novel (S/M) fusion, encoding a mosaic protein composed of the N-terminal 33 amino acids of Tet(S), in-frame with the Tet(M) coding sequence. Heterologous expression of the mosaic gene was found to confer Tet resistance upon recipients. Moreover, the (S/M) gene was found to be transcriptionally inducible by Tet under the endogenous (S) promoter in both and Nucleotide sequencing of the surrounding genomic region of 16.2 kb revealed large blocks of homology with the genomes of and A subregion of about 4 kb containing mosaic (S/M) was flanked by two copies of the IS mobile element. PCR amplification with primers directed outwards from the (S/M) gene identified the presence of a 4.3 kb circular form corresponding to the intervening chromosomal region between the two IS elements, but lacking a replication origin. The circular element shared extensive overall homology with a region of the multidrug-resistance plasmid pK214 from , containing (S), as well as the IS transposase-containing element and intervening non-coding sequences. Linear reconstruction of the insertion events likely to have occurred within this genomic region, inferred from sequence homology, provides further evidence of the chromosomal rearrangements that drive genomic evolution in complex bacterial communities such as the gut and food microbiota.

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2012-09-01
2020-08-04
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References

  1. Al-Jashamy K., Murad A., Zeehaida M., Rohaini M., Hasnan J.. ( 2010;). Prevalence of colorectal cancer associated with Streptococcus bovis among inflammatory bowel and chronic gastrointestinal tract disease patients. Asian Pac J Cancer Prev11:1765–1768[PubMed]
    [Google Scholar]
  2. Ammor M. S., Flórez A. B., Mayo B.. ( 2007;). Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacteria. Food Microbiol24:559–570 [CrossRef][PubMed]
    [Google Scholar]
  3. Berens C., Hillen W.. ( 2003;). Gene regulation by tetracyclines. Constraints of resistance regulation in bacteria shape TetR for application in eukaryotes. Eur J Biochem270:3109–3121 [CrossRef][PubMed]
    [Google Scholar]
  4. Boleij A., Schaeps R. M., Tjalsma H.. ( 2009;). Association between Streptococcus bovis and colon cancer. J Clin Microbiol47:516 [CrossRef][PubMed]
    [Google Scholar]
  5. Bouvet A., Grimont F., Collins M. D., Benaoudia F., Devine C., Regnault B., Grimont P. A.. ( 1997;). Streptococcus infantarius sp. nov. related to Streptococcus bovis and Streptococcus equinus. Adv Exp Med Biol418:393–395[PubMed]
    [Google Scholar]
  6. Celli J., Trieu-Cuot P.. ( 1998;). Circularization of Tn916 is required for expression of the transposon-encoded transfer functions: characterization of long tetracycline-inducible transcripts reading through the attachment site. Mol Microbiol28:103–117 [CrossRef][PubMed]
    [Google Scholar]
  7. Churchward G.. ( 2002;). Conjugative transposons and related mobile elements. Mobile DNA II Craig N., Craigie R., Gellert M.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  8. Clewell D. B., Flannagan S. E., Jaworski D. D., Clewell D. B.. ( 1995;). Unconstrained bacterial promiscuity: the Tn916–Tn1545 family of conjugative transposons. Trends Microbiol3:229–236 [CrossRef][PubMed]
    [Google Scholar]
  9. Comunian R., Daga E., Dupré I., Paba A., Devirgiliis C., Piccioni V., Perozzi G., Zonenschain D., Rebecchi A.. & other authors ( 2010;). Susceptibility to tetracycline and erythromycin of Lactobacillus paracasei strains isolated from traditional Italian fermented foods. Int J Food Microbiol138:151–156 [CrossRef][PubMed]
    [Google Scholar]
  10. Devirgiliis C., Caravelli A., Coppola D., Barile S., Perozzi G.. ( 2008;). Antibiotic resistance and microbial composition along the manufacturing process of Mozzarella di Bufala Campana. Int J Food Microbiol128:378–384 [CrossRef][PubMed]
    [Google Scholar]
  11. Devirgiliis C., Coppola D., Barile S., Colonna B., Perozzi G.. ( 2009;). Characterization of the Tn916 conjugative transposon in a food-borne strain of Lactobacillus paracasei. Appl Environ Microbiol75:3866–3871 [CrossRef][PubMed]
    [Google Scholar]
  12. Devirgiliis C., Barile S., Caravelli A., Coppola D., Perozzi G.. ( 2010;). Identification of tetracycline- and erythromycin-resistant Gram-positive cocci within the fermenting microflora of an Italian dairy food product. J Appl Microbiol109:313–323[PubMed]
    [Google Scholar]
  13. Facklam R.. ( 2002;). What happened to the streptococci: overview of taxonomic and nomenclature changes. Clin Microbiol Rev15:613–630 [CrossRef][PubMed]
    [Google Scholar]
  14. Farrow J. A., Collins M. D.. ( 1984;). DNA base composition, DNA–DNA homology and long-chain fatty acid studies on Streptococcus thermophilus and Streptococcus salivarius. J Gen Microbiol130:357–362[PubMed]
    [Google Scholar]
  15. Fernández-Ruiz M., Villar-Silva J., Llenas-García J., Caurcel-Díaz L., Vila-Santos J., Sanz-Sanz F., Chaves F., Guerra-Vales J. M.. ( 2010;). Streptococcus bovis bacteraemia revisited: clinical and microbiological correlates in a contemporary series of 59 patients. J Infect61:307–313 [CrossRef][PubMed]
    [Google Scholar]
  16. Flórez A. B., Ammor M. S., Mayo B.. ( 2008;). Identification of tet(M) in two Lactococcus lactis strains isolated from a Spanish traditional starter-free cheese made of raw milk and conjugative transfer of tetracycline resistance to lactococci and enterococci. Int J Food Microbiol121:189–194 [CrossRef][PubMed]
    [Google Scholar]
  17. Freitas A. R., Coque T. M., Novais C., Hammerum A. M., Lester C. H., Zervos M. J., Donabedian S., Jensen L. B., Francia M. V.. & other authors ( 2011;). Human and swine hosts share vancomycin-resistant Enterococcus faecium CC17 and CC5 and Enterococcus faecalis CC2 clonal clusters harboring Tn1546 on indistinguishable plasmids. J Clin Microbiol49:925–931 [CrossRef][PubMed]
    [Google Scholar]
  18. Garrett W. S., Gallini C. A., Yatsunenko T., Michaud M., DuBois A., Delaney M. L., Punit S., Karlsson M., Bry L.. & other authors ( 2010;). Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe8:292–300 [CrossRef][PubMed]
    [Google Scholar]
  19. Gueguen E., Rousseau P., Duval-Valentin G., Chandler M.. ( 2006;). Truncated forms of IS911 transposase downregulate transposition. Mol Microbiol62:1102–1116 [CrossRef][PubMed]
    [Google Scholar]
  20. Gupta A., Madani R., Mukhtar H.. ( 2010;). Streptococcus bovis endocarditis, a silent sign for colonic tumour. Colorectal Dis12:164–171 [CrossRef][PubMed]
    [Google Scholar]
  21. Herrera P., Kwon Y. M., Ricke S. C.. ( 2009;). Ecology and pathogenicity of gastrointestinal Streptococcus bovis. Anaerobe15:44–54 [CrossRef][PubMed]
    [Google Scholar]
  22. Kahveci A., Ari E., Arikan H., Koc M., Tuglular S., Ozener C.. ( 2010;). Streptococcus bovis bacteremia related to colon adenoma in a chronic hemodialysis patient. Hemodial Int14:91–93 [CrossRef][PubMed]
    [Google Scholar]
  23. Kazimierczak K. A., Flint H. J., Scott K. P.. ( 2006;). Comparative analysis of sequences flanking tet(W) resistance genes in multiple species of gut bacteria. Antimicrob Agents Chemother50:2632–2639 [CrossRef][PubMed]
    [Google Scholar]
  24. Mahillon J., Chandler M.. ( 1998;). Insertion sequences. Microbiol Mol Biol Rev62:725–774[PubMed]
    [Google Scholar]
  25. Moet G. J., Dowzicky M. J., Jones R. N.. ( 2007;). Tigecycline (GAR-936) activity against Streptococcus gallolyticus (bovis) and viridans group streptococci. Diagn Microbiol Infect Dis57:333–336 [CrossRef][PubMed]
    [Google Scholar]
  26. Novais C., Freitas A. R., Sousa J. C., Baquero F., Coque T. M., Peixe L. V.. ( 2008;). Diversity of Tn1546 and its role in the dissemination of vancomycin-resistant enterococci in Portugal. Antimicrob Agents Chemother52:1001–1008 [CrossRef][PubMed]
    [Google Scholar]
  27. Ogier J. C., Serror P.. ( 2008;). Safety assessment of dairy microorganisms: the Enterococcus genus. Int J Food Microbiol126:291–301 [CrossRef][PubMed]
    [Google Scholar]
  28. Patterson A. J., Rincon M. T., Flint H. J., Scott K. P.. ( 2007;). Mosaic tetracycline resistance genes are widespread in human and animal fecal samples. Antimicrob Agents Chemother51:1115–1118 [CrossRef][PubMed]
    [Google Scholar]
  29. Paulsen I. T., Banerjei L., Myers G. S., Nelson K. E., Seshadri R., Read T. D., Fouts D. E., Eisen J. A., Gill S. R.. & other authors ( 2003;). Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science299:2071–2074 [CrossRef][PubMed]
    [Google Scholar]
  30. Perreten V., Schwarz F., Cresta L., Boeglin M., Dasen G., Teuber M.. ( 1997;). Antibiotic resistance spread in food. Nature389:801–802 [CrossRef][PubMed]
    [Google Scholar]
  31. Pilhofer M., Bauer A. P., Schrallhammer M., Richter L., Ludwig W., Schleifer K. H., Petroni G.. ( 2007;). Characterization of bacterial operons consisting of two tubulins and a kinesin-like gene by the novel two-step gene walking method. Nucleic Acids Res35:e135 [CrossRef][PubMed]
    [Google Scholar]
  32. Roberts A. P., Mullany P.. ( 2009;). A modular master on the move: the Tn916 family of mobile genetic elements. Trends Microbiol17:251–258 [CrossRef][PubMed]
    [Google Scholar]
  33. Schlegel L., Grimont F., Collins M. D., Régnault B., Grimont P. A., Bouvet A.. ( 2000;). Streptococcus infantarius sp. nov., Streptococcus infantarius subsp. infantarius subsp. nov. and Streptococcus infantarius subsp. coli subsp. nov., isolated from humans and food. Int J Syst Evol Microbiol50:1425–1434 [CrossRef][PubMed]
    [Google Scholar]
  34. Schlegel L., Grimont F., Ageron E., Grimont P. A., Bouvet A.. ( 2003;). Reappraisal of the taxonomy of the Streptococcus bovis/Streptococcus equinus complex and related species: description of Streptococcus gallolyticus subsp. gallolyticus subsp. nov., S. gallolyticus subsp. macedonicus subsp. nov. and S. gallolyticus subsp. pasteurianus subsp. nov. Int J Syst Evol Microbiol53:631–645 [CrossRef][PubMed]
    [Google Scholar]
  35. Schlegel L., Grimont F., Grimont P. A., Bouvet A.. ( 2004;). New group D streptococcal species. Indian J Med Res119:Suppl.252–256[PubMed]
    [Google Scholar]
  36. Siezen R. J., Bayjanov J., Renckens B., Wels M., van Hijum S. A., Molenaar D., van Hylckama Vlieg J. E.. ( 2010;). Complete genome sequence of Lactococcus lactis subsp. lactis KF147, a plant-associated lactic acid bacterium. J Bacteriol192:2649–2650 [CrossRef][PubMed]
    [Google Scholar]
  37. Srivastava A., Walter N., Atkinson P.. ( 2010;). Streptococcus bovis infection of total hip arthroplasty in association with carcinoma of colon. J Surg Orthop Adv19:125–128[PubMed]
    [Google Scholar]
  38. Stanton T. B., Humphrey S. B., Scott K. P., Flint H. J.. ( 2005;). Hybrid tet genes and tet gene nomenclature: request for opinion. Antimicrob Agents Chemother49:1265–1266 [CrossRef][PubMed]
    [Google Scholar]
  39. Su Y. A., He P., Clewell D. B.. ( 1992;). Characterization of the tet(M) determinant of Tn916: evidence for regulation by transcription attenuation. Antimicrob Agents Chemother36:769–778 [CrossRef][PubMed]
    [Google Scholar]
  40. Tsai J. C., Hsueh P. R., Chen H. J., Tseng S. P., Chen P. Y., Teng L. J.. ( 2005;). The erm(T) gene is flanked by IS1216V in inducible erythromycin-resistant Streptococcus gallolyticus subsp. pasteurianus. Antimicrob Agents Chemother49:4347–4350 [CrossRef][PubMed]
    [Google Scholar]
  41. van Hoek A. H., Mayrhofer S., Domig K. J., Flórez A. B., Ammor M. S., Mayo B., Aarts H. J.. ( 2008;). Mosaic tetracycline resistance genes and their flanking regions in Bifidobacterium thermophilum and Lactobacillus johnsonii. Antimicrob Agents Chemother52:248–252 [CrossRef][PubMed]
    [Google Scholar]
  42. Wozniak R. A., Waldor M. K.. ( 2010;). Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol8:552–563 [CrossRef][PubMed]
    [Google Scholar]
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