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Volume 154, Issue 10

Vancomycin heteroresistance and biofilm formation in from food Free

Abstract

CNBL 7032 is a heteroresistant strain, with subpopulations resistant to vancomycin concentrations up to 32 mg l , which was isolated from cured pork meat. The mechanisms of glycopeptide resistance in this strain were investigated in this study. CNBL 7032 does not harbour enterococcal transmissible vancomycin-resistance genes. Transmission electron microscopy revealed that resistant subpopulations have a thicker cell wall, and that the increase in cell wall thickness is proportional to vancomycin concentration in the growth medium. Scanning electron microscopy showed that CNBL 7032 forms a biofilm-like structure when grown in the presence of vancomycin. This food isolate harbours the gene coding for an autolysin with an adhesive function, which is involved in the first phase of biofilm formation. This study has demonstrated an interaction between expression, biofilm formation and glycopeptide antibiotic resistance; transcription analysis demonstrated that the expression of increased proportionally with the vancomycin concentration in the culture. Insertional inactivation of confirmed the role of the AtlE autolysin in biofilm and vancomycin resistance.

  • Received:
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Keyword(s): CNS, coagulase-negative staphylococci , PIA, polysaccharide intercellular adhesin , RTq-PCR, quantitative reverse transcriptase polymerase chain reaction , SEM, scanning electron microscopy and TEM, transmisison electron microscopy
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2008-10-01
2024-04-23
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References

  1. Augustin J., Gotz F. 1990; Transformation of Staphylococcus epidermidis and other staphylococcal species with plasmid DNA by electroporation. FEMS Microbiol Lett 54:203–207
     [Google Scholar]
  2. Berger-Bachi B., Strassle A., Gustafson J. E., Kayser F. H. 1992; Mapping and characterization of multiple chromosomal factors involved in methicillin resistance in Staphylococcus aureus . Antimicrob Agents Chemother 36:1367–1373
     [Google Scholar]
  3. Biavasco F., Vignaroli C., Varaldo P. E. 2000; Glycopeptide resistance in coagulase-negative staphylococci. Eur J Clin Microbiol Infect Dis 19:403–417
     [Google Scholar]
  4. Bover-Cid S., Izquierdo-Pulido M., Vidal-Carou M. C. 1999; Effect of proteolytic starter cultures of Staphylococcus spp. on biogenic amine formation during the ripening of dry fermented sausages. Int J Food Microbiol 46:95–104
     [Google Scholar]
  5. Bover-Cid S., Izquierdo-Pulido M., Vidal-Carou M. C. 2000; Mixed starter cultures to control biogenic amine production in dry fermented sausages. J Food Prot 63:1556–1562
     [Google Scholar]
  6. Boyle-Vavra S., Carey R. B., Daum R. S. 2001; Development of vancomycin and lysostaphin resistance in a methicillin-resistant Staphylococcus aureus isolate. J Antimicrob Chemother 48:617–625
     [Google Scholar]
  7. Chen Y., McClane B. A., Fisher D. J., Rood J. I., Gupta P. 2005; Construction of an alpha toxin gene knockout mutant of Clostridium perfringens type A by use of a mobile group II intron. Appl Environ Microbiol 71:7542–7547
     [Google Scholar]
  8. Clark N. C., Cooksey R. C., Hill B. C., Swenson J. M., Tenover F. C. 1993; Characterization of glycopeptide-resistant enterococci from U.S. hospitals. Antimicrob Agents Chemother 37:2311–2317
     [Google Scholar]
  9. Cocconcelli P. S., Porro D., Galandini S., Senini L. 1995; Development of RAPD protocol for typing of strains of lactic acid bacteria and enterococci. Lett Appl Microbiol 21:376–379
     [Google Scholar]
  10. Cui L., Ma X., Sato K., Okuma K., Tenover F. C., Mamizuka E. M., Gemmell C. G., Kim M., Ploy M. other authors 2003; Cell wall thickening is a common feature of vancomycin resistance in Staphylococcus aureus . J Clin Microbiol 41:5–14
     [Google Scholar]
  11. Eleaume H., Jabbouri S. 2004; Comparison of two standardisation methods in real-time quantitative RT-PCR to follow Staphylococcus aureus genes expression during in vitro growth. J Microbiol Methods 59:363–370
     [Google Scholar]
  12. Flannagan S. E., Chow J. W., Donabedian S. M., Brown W. J., Perri M. B., Zervos M. J., Ozawa Y., Clewell D. B. 2003; Plasmid content of a vancomycin-resistant Enterococcus faecalis isolate from a patient also colonized by Staphylococcus aureus with a VanA phenotype. Antimicrob Agents Chemother 47:3954–3959
     [Google Scholar]
  13. Geisel R., Schmitz F. J., Thomas L., Berns G., Zetsche O., Ulrich B., Fluit A. C., Labischinsky H., Witte W. 1999; Emergence of heterogeneous intermediate vancomycin resistance in Staphylococcus aureus isolates in the Dusseldorf area. J Antimicrob Chemother 43:846–848
     [Google Scholar]
  14. Götz F. 2002; Staphylococcus and biofilm. Mol Microbiol 43:1367–1378
     [Google Scholar]
  15. Hanaki H., Kuwahara-Arai K., Boyle-Vavra S., Daum R. S., Labischinski H., Himaratsu K. 1998; Activated cell-wall synthesis is associated with vancomycin resistance in methicillin-resistant Staphylococcus aureus clinical strains Mu3 and Mu50. J Antimicrob Chemother 42:199–209
     [Google Scholar]
  16. Heilmann C., Hussain M., Peters G., Götz F. 1997; Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 24:1013–1024
     [Google Scholar]
  17. Heilmann C., Thumm G., Chhatwal G. S., Hartleib J., Uekotter A., Peters G. 2003; Identification and characterization of a novel autolysin (Aae) with adhesive properties from Staphylococcus epidermidis . Microbiology 149:2769–2778
     [Google Scholar]
  18. Hiramatsu K., Aritaka N., Hanaki H., Kawasaki S., Hosoda Y., Hori S., Yoshinosuke F., Kobayashi I. 1997; Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet 350:1670–1673
     [Google Scholar]
  19. Jefferson K. K., Pier D. B., Goldmann D. A., Pier G. B. 2004; The teicoplanin-associated locus regulator (TcaR) and the intercellular adhesion locus regulator (IcaR) are transcriptional inhibitors of the ica locus in Staphylococcus aureus . J Bacteriol 186:2449–2456
     [Google Scholar]
  20. Kodjikian L., Burillon C., Roques C., Pellon G., Freney J., Renaud F. N. 2003a; Biofilm formation on intraocular lenses by a clinical strain encoding the ica locus: a scanning electron microscopy study. Invest Ophthalmol Vis Sci 44:4382–4387
     [Google Scholar]
  21. Kodjikian L., Burillon C., Lina G., Roques C., Pellon G., Freney J., Renaud F. N. 2003b; Bacterial adherence of Staphylococcus epidermidis to intraocular lenses: a bioluminescence and scanning electron microscopy study. Invest Ophthalmol Vis Sci 44:4388–4394
     [Google Scholar]
  22. Livermore D. M. 2000; Antibiotic resistance in staphylococci. Int J Antimicrob Agents 16:S3–S10
     [Google Scholar]
  23. Maidak B. L., Cole J. R., Lilburn T. G., Parker C. T. Jr, Saxman P. R., Farris R. J., Garrity G. M., Olsen G. J., Schmidt T. M., Tiedje J. M. 2001; The RDP-II (Ribosomal Database Project. Nucleic Acids Res 29:173–174
     [Google Scholar]
  24. Mønzøn M., Oteiza C., Leiva J., Lamata M., Amorena B. 2002; Biofilm testing of Staphylococcus epidermidis clinical isolates: low performance of vancomycin in relation to other antibiotics. Diagn Microbiol Infect Dis 44:319–324
     [Google Scholar]
  25. NCCLS 2000 Perfomance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals , 2nd edn. Approved Standard M31-A2. Villanova, PA: NCCLS;
     [Google Scholar]
  26. Noble W. C., Virani Z., Cree R. G. 1992; Co-transfer of vancomycin and other resistance genes from Enterococcus faecalis NCTC 12201 to Staphylococcus aureus . FEMS Microbiol Lett 72:195–198
     [Google Scholar]
  27. Nunes A. P., Teixeira L. M., Iorio N. L., Bastos C. C., de Sousa Fonseca L., Souto-Padrón T., dos Santos K. R. 2006; Heterogeneous resistance to vancomycin in Staphylococcus epidermidis, Staphylococcus haemolyticus and Staphylococcus warneri clinical strains: characterisation of glycopeptide susceptibility profiles and cell wall thickening. Int J Antimicrob Agents 27:307–315
     [Google Scholar]
  28. O'Gara J. P. 2007; ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus . FEMS Microbiol Lett 270:179–188
     [Google Scholar]
  29. Qin Z., Ou Y., Yang L., Zhu Y., Tolker-Nielsen T., Molin S., Qu D. 2007; Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis . Microbiology 153:2083–2092
     [Google Scholar]
  30. Reipert A., Ehlert K., Kast T., Bierbaum G. 2003; Morphological and genetic differences in two isogenic Staphylococcus aureus strains with decreased susceptibilities to vancomycin. Antimicrob Agents Chemother 47:568–576
     [Google Scholar]
  31. Rice L. B. 2006; Antimicrobial resistance in gram positive bacteria. Am J Infect Control 34 :Suppl. 1S11–S19
     [Google Scholar]
  32. Rozen S., Skaletsky H. 2000; Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386
     [Google Scholar]
  33. Rupp M. E., Fey P. D., Heilmann C., Götz F. 2001; Characterization of the importance of Staphylococcus epidermidis autolysin and polysaccharide intercellular adhesin in the pathogenesis of intravascular catheter-associated infection in a rat model. J Infect Dis 183:1038–1042
     [Google Scholar]
  34. Showsh S. A., De Boever E. H., Clewell D. B. 2001; Vancomycin resistance plasmid in Enterococcus faecalis that encodes sensitivity to a sex pheromone also produced by Staphylococcus aureus . Antimicrob Agents Chemother 45:2177–2178
     [Google Scholar]
  35. Siebert W. T., Moreland N., Williams T. W. Jr 1979; Synergy of vancomycin plus cefazolin or cephalothin against methicillin-resistance Staphylococcus epidermidis . J Infect Dis 139:452–457
     [Google Scholar]
  36. Sieradzki K., Tomasz A. 2003; Alterations of cell wall structure and metabolism accompany reduced susceptibility to vancomycin in an isogenic series of clinical isolates of Staphylococcus aureus . J Bacteriol 185:7103–7110
     [Google Scholar]
  37. Sondergaard A. K., Stahnke L. H. 2002; Growth and aroma production by Staphylococcus xylosus, S. carnosus and S. equorum: a comparative study in model systems. Int J Food Microbiol 75:99–109
     [Google Scholar]
  38. Srinivasan A., Dick J. D., Perl T. M. 2002; Vancomycin resistance in staphylococci. Clin Microbiol Rev 15:430–438
     [Google Scholar]
  39. Vandecasteele S. J., Peetermans W. E., Merckx R., Van Eldere J. 2003; Expression of biofilm-associated genes in Staphylococcus epidermidis during in vitro and in vivo foreign body infections. J Infect Dis 188:730–737
     [Google Scholar]
  40. Van Der Zwet W. C., Derbets-Ossenkopp Y. J., Reinders E., Kapi M., Savelkoul P. H. M., Van Elburg R. M., Hiramatsu K., Vandenbroucke-Grauls C. M. J. E. 2002; Nosocomial spread of a Staphylococcus capitis strain with heteroresistance to vancomycin in a neonatal intensive care unit. J Clin Microbiol 40:2520–2525
     [Google Scholar]
  41. Vilar I., Garcia Fontan M. C., Prieto B., Tornadijo M. E., Carballo J. 2000; A survey on the microbiological changes during the manufacture of dry-cured lacón, a Spanish traditional meat product. J Appl Microbiol 89:1018–1026
     [Google Scholar]
  42. Von Eiff C., Peters G., Heilmann C. 2002; Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2:677–685
     [Google Scholar]
  43. Vuong C., Gerke C., Somerville G. A., Fischer E. R., Otto M. 2003; Quorum-sensing control of biofilm factors in Staphylococcus epidermidis . J Infect Dis 188:706–718
     [Google Scholar]
  44. Yao Y., Sturdevant D. E., Otto M. 2005; Genomewide analysis of gene expression in Staphylococcus epidermidis biofilms: insights into the pathophysiology of S. epidermidis biofilms and the role of phenol-soluble modulins in formation of biofilms. J Infect Dis 191:289–298
     [Google Scholar]
  45. Ziebuhr W., Krimmer V., Rachid S., Lossner I., Götz F., Hacker J. 1999; A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesion synthesis by alternating insertion and excision of the insertion sequence element IS 256 . Mol Microbiol 32:345–356
     [Google Scholar]
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Vancomycin heteroresistance and biofilm formation in Staphylococcus epidermidis from food
Microbiology 154, 3224 (2008); https://doi.org/10.1099/mic.0.2008/021154-0
/content/journal/micro/10.1099/mic.0.2008/021154-0
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