1887

Journal of Medical Microbiology logo

Volume 62, Issue 3

Effects of efflux-pump inducers and genetic variation of the multidrug transporter in biocide resistance of and Free

Abstract

Multidrug efflux pumps, such as CmeABC and CmeDEF, are involved in the resistance of to a broad spectrum of antimicrobials. The aim of this study was to analyse the effects of two putative efflux-pump inducers, bile salts and sodium deoxycholate, on the resistance of to biocides (triclosan, benzalkonium chloride, chlorhexidine diacetate, cetylpyridinium chloride and trisodium phosphate), SDS and erythromycin. The involvement of the CmeABC and CmeDEF efflux pumps in this resistance was studied on the basis of the effects of bile salts and sodium deoxycholate in , and mutants. The genetic variation in the gene was also examined, to see whether this polymorphism is related to the function of the efflux pump. In 15 and 23 strains, bile salts and sodium deoxycholate increased the MICs of benzalkonium chloride, chlorhexidine diacetate, cetylpyridinium chloride and SDS, and decreased the MICs of triclosan, trisodium phosphate and erythromycin. Bile salts and sodium deoxycholate further decreased or increased the MICs of biocides and erythromycin in the and mutants. For polymorphisms, 17 different specific PCR-RFLP patterns were identified: six within only, nine within only and two in both species. In conclusion, bile salts and sodium deoxycholate can increase or decrease bacterial resistance to structurally unrelated antimicrobials. The MIC increases in the and mutants indicated that at least one non-CmeABC efflux system is involved in resistance to biocides. These results indicate that the gene polymorphism identified is not associated with biocide and erythromycin resistance in .

  • Received:
  • Accepted:
  • Published Online:
© 2013 SGM
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.052316-0
2013-03-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jmm/62/3/400.html?itemId=/content/journal/jmm/10.1099/jmm.0.052316-0&mimeType=html&fmt=ahah

References

  1. Akiba M., Lin J., Barton Y.-W., Zhang Q. 2006; Interaction of CmeABC and CmeDEF in conferring antimicrobial resistance and maintaining cell viability in Campylobacter jejuni . J Antimicrob Chemother 57:52–60 [View Article][PubMed]
     [Google Scholar]
  2. Amaral L., Engi H., Viveiros M., Molnar J. 2007; Comparison of multidrug resistant efflux pumps of cancer and bacterial cells with respect to the same inhibitory agents. In Vivo 21:237–244[PubMed]
     [Google Scholar]
  3. Amaral L., Fanning S., Pagès J. M. 2011; Efflux pumps of Gram-negative bacteria: genetic responses to stress and the modulation of their activity by pH, inhibitors, and phenothiazines. Adv Enzymol Relat Areas Mol Biol 77:61–108 [View Article][PubMed]
     [Google Scholar]
  4. Braoudaki M., Hilton A. C. 2005; Mechanisms of resistance in Salmonella enterica adapted to erythromycin, benzalkonium chloride and triclosan. Int J Antimicrob Agents 25:31–37 [View Article][PubMed]
     [Google Scholar]
  5. Cagliero C., Cloix L., Cloeckaert A., Payot S. 2006; High genetic variation in the multidrug transporter cmeB gene in Campylobacter jejuni and Campylobacter coli . J Antimicrob Chemother 58:168–172 [View Article][PubMed]
     [Google Scholar]
  6. Caldwell D. B., Wang Y., Lin J. 2008; Development, stability, and molecular mechanisms of macrolide resistance in Campylobacter jejuni . Antimicrob Agents Chemother 52:3947–3954 [View Article][PubMed]
     [Google Scholar]
  7. Chopra I., O’Neill A. J., Miller K. 2003; The role of mutators in the emergence of antibiotic-resistant bacteria. Drug Resist Updat 6:137–145 [View Article][PubMed]
     [Google Scholar]
  8. CLSI 2007; Performance Standards for Antimicrobial Susceptibility Testing. Sixteenth Informational Supplement M100–S16. Wayne, PA: Clinical and Laboratory Standards Institute;
  9. Dorrell N., Mangan J. A., Laing K. G., Hinds J., Linton D., Al-Ghusein H., Barrell B. G., Parkhill J., Stoker N. G. other authors 2001; Whole genome comparison of Campylobacter jejuni human isolates using a low-cost microarray reveals extensive genetic diversity. Genome Res 11:1706–1715 [View Article][PubMed]
     [Google Scholar]
  10. Gibreel A., Kos V. N., Keelan M., Trieber C. A., Levesque S., Michaud S., Taylor D. E. 2005; Macrolide resistance in Campylobacter jejuni and Campylobacter coli: molecular mechanism and stability of the resistance phenotype. Antimicrob Agents Chemother 49:2753–2759 [View Article][PubMed]
     [Google Scholar]
  11. Hannula M., Hänninen M.-L. 2008; Effect of putative efflux pump inhibitors and inducers on the antimicrobial susceptibility of Campylobacter jejuni and Campylobacter coli . J Med Microbiol 57:851–855 [View Article][PubMed]
     [Google Scholar]
  12. Jayaraman R. 2011; Hypermutation and stress adaptation in bacteria. J Genet 90:383–391 [View Article][PubMed]
     [Google Scholar]
  13. Jeon B., Wang Y., Hao H., Barton Y. W., Zhang Q. 2011; Contribution of CmeG to antibiotic and oxidative stress resistance in Campylobacter jejuni . J Antimicrob Chemother 66:79–85 [View Article][PubMed]
     [Google Scholar]
  14. Kern W. V., Steinke P., Schumacher A., Schuster S., von Baum H., Bohnert J. A. 2006; Effect of 1-(1-naphthylmethyl)-piperazine, a novel putative efflux pump inhibitor, on antimicrobial drug susceptibility in clinical isolates of Escherichia coli . J Antimicrob Chemother 57:339–343 [View Article][PubMed]
     [Google Scholar]
  15. Kim J.-S., Carver D. K., Kathariou S. 2006; Natural transformation-mediated transfer of erythromycin resistance in Campylobacter coli strains from turkeys and swine. Appl Environ Microbiol 72:1316–1321 [View Article][PubMed]
     [Google Scholar]
  16. Klančnik A., Botteldoorn N., Herman L., Smole Možina S. 2006; Survival and stress induced expression of groEL and rpoD of Campylobacter jejuni from different growth phases. Int J Food Microbiol 112:200–207 [View Article][PubMed]
     [Google Scholar]
  17. Klančnik A., Smole Možina S., Zhang Q. 2012; Anti-Campylobacter activities and resistance mechanisms of natural phenolic compounds in Campylobacter . PLoS One 7:e51800 [View Article][PubMed]
     [Google Scholar]
  18. Kurinčič M. 2011 Mechanisms of resistance of Campylobacter jejuni and Campylobacter coli against selected antimicrobials. PhD thesis, Biotechnical Faculty, Ljubljana, Slovenia
  19. Kurinčič M., Botteldoorn N., Herman L., Smole Možina S. 2007; Mechanisms of erythromycin resistance of Campylobacter spp. isolated from food, animals and humans. Int J Food Microbiol 120:186–190 [View Article][PubMed]
     [Google Scholar]
  20. Leser T. D., Møller K., Jensen T. K., Jorsal S. E. 1997; Specific detection of Serpulina hyodysenteriae and potentially pathogenic weakly β-haemolytic porcine intestinal spirochetes by polymerase chain reaction targeting 23S rDNA. Mol Cell Probes 11:363–372 [View Article][PubMed]
     [Google Scholar]
  21. Li X.-Z., Nikaido H. 2004; Efflux-mediated drug resistance in bacteria. Drugs 64:159–204 [View Article][PubMed]
     [Google Scholar]
  22. Lin J., Michel L. O., Zhang Q. 2002; CmeABC functions as a multidrug efflux system in Campylobacter jejuni . Antimicrob Agents Chemother 46:2124–2131 [View Article][PubMed]
     [Google Scholar]
  23. Lin J., Akiba M., Sahin O., Zhang Q. 2005a; CmeR functions as a transcriptional repressor for the multidrug efflux pump CmeABC in Campylobacter jejuni . Antimicrob Agents Chemother 49:1067–1075 [View Article][PubMed]
     [Google Scholar]
  24. Lin J., Cagliero C., Guo B., Barton Y. W., Maurel M. C., Payot S., Zhang Q. 2005b; Bile salts modulate expression of the CmeABC multidrug efflux pump in Campylobacter jejuni . J Bacteriol 187:7417–7424 [View Article][PubMed]
     [Google Scholar]
  25. Luangtongkum T., Jeon B., Han J., Plummer P., Logue C. M., Zhang Q. 2009; Antibiotic resistance in Campylobacter: emergence, transmission and persistence. Future Microbiol 4:189–200 [View Article][PubMed]
     [Google Scholar]
  26. Martinez A. D. L., Lin J. 2006; Effect of an efflux pump inhibitor on the function of the multidrug efflux pump CmeABC and antimicrobial resistance in Campylobacter . Foodborne Pathog Dis 3:393–402 [View Article][PubMed]
     [Google Scholar]
  27. Martins A., Couto I., Aagaard L., Martins M., Viveiros M., Kristiansen J. E., Amaral L. 2007; Prolonged exposure of methicillin-resistant Staphylococcus aureus (MRSA) COL strain to increasing concentrations of oxacillin results in a multidrug-resistant phenotype. Int J Antimicrob Agents 29:302–305 [View Article][PubMed]
     [Google Scholar]
  28. Martins A., Iversen C., Rodrigues L., Spengler G., Ramos J., Kern W. V., Couto I., Viveiros M., Fanning S. other authors 2009a; An AcrAB-mediated multidrug-resistant phenotype is maintained following restoration of wild-type activities by efflux pump genes and their regulators. Int J Antimicrob Agents 34:602–604 [View Article][PubMed]
     [Google Scholar]
  29. Martins A., Spengler G., Rodrigues L., Viveiros M., Ramos J., Martins M., Couto I., Fanning S., Pagès J. M. other authors 2009b; pH Modulation of efflux pump activity of multi-drug resistant Escherichia coli: protection during its passage and eventual colonization of the colon. PLoS ONE 4:e6656 [View Article][PubMed]
     [Google Scholar]
  30. Mavri A., Smole Možina S. 2012; Involvement of efflux mechanisms in biocide resistance of Campylobacter jejuni and Campylobacter coli . J Med Microbiol 61:800–808 [View Article][PubMed]
     [Google Scholar]
  31. Meyer B., Cookson B. 2010; Does microbial resistance or adaptation to biocides create a hazard in infection prevention and control?. J Hosp Infect 76:200–205 [View Article][PubMed]
     [Google Scholar]
  32. Moore J. E., Barton M. D., Blair I. S., Corcoran D., Dooley J. S. G., Fanning S., Kempf I., Lastovica A. J., Lowery C. J. other authors 2006; The epidemiology of antibiotic resistance in Campylobacter . Microbes Infect 8:1955–1966 [View Article][PubMed]
     [Google Scholar]
  33. Park S. F. 2002; The physiology of Campylobacter species and its relevance to their role as foodborne pathogens. Int J Food Microbiol 74:177–188 [View Article][PubMed]
     [Google Scholar]
  34. Parkhill J., Wren B. W., Mungall K., Ketley J. M., Churcher C., Basham D., Chillingworth T., Davies R. M., Feltwell T. other authors 2000; The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665–668 [View Article][PubMed]
     [Google Scholar]
  35. Pumbwe L., Randall L. P., Woodward M. J., Piddock L. J. 2005; Evidence for multiple-antibiotic resistance in Campylobacter jejuni not mediated by CmeB or CmeF. Antimicrob Agents Chemother 49:1289–1293 [View Article][PubMed]
     [Google Scholar]
  36. Russell A. D. 2002; Introduction of biocides into clinical practice and the impact on antibiotic-resistant bacteria. Symp Ser Soc Appl Microbiol 92:121S–135S[PubMed] [CrossRef]
     [Google Scholar]
  37. Smulders E., Rybinski W., Sung E., Rähse W., Steber J., Wiebel F., Nordskog A. 2002; Laundry detergents. In Ullmann’s Encyclopedia of Industrial Chemistry p. 315 Edited by Elvers B. Weinheim: Wiley-VCH;
     [Google Scholar]
  38. Zhang Q., Sahin O., McDermott P. F., Payot S. 2006; Fitness of antimicrobial-resistant Campylobacter and Salmonella . Microbes Infect 8:1972–1978 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.052316-0
Loading
Effects of efflux-pump inducers and genetic variation of the multidrug transporter cmeB in biocide resistance of Campylobacter jejuni and Campylobacter coli
J. Med. Microbiol. 62, 400 (2013); https://doi.org/10.1099/jmm.0.052316-0
/content/journal/jmm/10.1099/jmm.0.052316-0
/content/journal/jmm/10.1099/jmm.0.052316-0
Loading

Data & Media loading...

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