1887

Abstract

Strains of the food-borne pathogen , showing either intermediate or high-level resistance to class IIa bacteriocins, were investigated to determine characteristics that correlated with their sensitivity levels. Two intermediate and one highly resistant spontaneous mutant of B73, a highly resistant mutant of 412, and a highly resistant, defined () mutant of EGDe were compared with their respective wild-type strains in order to investigate the contribution of different factors to resistance. Decreased mannose-specific phosphotransferase system gene expression (, EIIAB component) was implicated in all levels of resistance, confirming previous studies by the authors' group. However, a clear correlation between -alanine content in teichoic acid (TA), in particular the alanine : phosphorus ratio, and a more positive cell surface, as determined by cytochrome binding, were found for the highly resistant strains. Furthermore, two of the three highly resistant strains showed a significant increase in sensitivity towards -cycloserine (DCS). However, real-time PCR of the (-alanine esterification), and and genes (peptidoglycan biosynthesis) showed no change in transcriptional levels. The link between DCS sensitivity and increased -alanine esterification of TA may be that DCS competes with alanine for transport via the alanine transporter. A possible tendency towards increased lysinylation of membrane phospholipid in the highly resistant strains was also found. A previous study reported that cell membranes of all the resistant strains, including the intermediate resistant strains, contained more unsaturated phosphatidylglycerol, which is an indication of a more fluid cell membrane. The results of that study correlate with the possible lysinylation, decreased expression, -alanine esterification of TA and more positive cell surface charge found in this study for resistant strains. The authors' findings strongly indicate that all these factors could contribute to class IIa bacteriocin resistance and that the combination and contribution of each of these factors determine the level of bacteriocin resistance.

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2004-09-01
2019-11-23
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References

  1. Abachin, E., Poyart, C., Pellegrini, E., Milohanic, E., Fiedler, F., Berche, P. & Trieu-Cuot, P. ( 2002; ). Formation of d-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol Microbiol 43, 1–14.[CrossRef]
    [Google Scholar]
  2. Ames, B. ( 1966; ). Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol 8, 115–118.
    [Google Scholar]
  3. Bidlingmeyer, B., Cohen, S. & Tarvin, T. ( 1984; ). Rapid analysis of amino acids using pre-column derivitization. J Chromatogr 336, 93–104.[CrossRef]
    [Google Scholar]
  4. Bierbaum, G. & Sahl, H.-G. ( 1987; ). Autolytic system of Staphylococcus simulans 22, influence of cationic peptides on activity of N-acetylmuramoyl-l-alanine amidase. J Bacteriol 169, 5452–5458.
    [Google Scholar]
  5. Bligh, E. G. & Dyer, W. J. ( 1959; ). A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37, 911–917.[CrossRef]
    [Google Scholar]
  6. Chen, Y., Shapiro, R., Eisenstein, M. & Montville, T. ( 1997; ). Functional characterization of pediocin PA-1 binding to liposomes in the absence of a protein receptor and its relationship to a predicted tertiary structure. Appl Environ Microbiol 63, 524–531.
    [Google Scholar]
  7. Crandall, A. D. & Montville, T. J. ( 1998; ). Nisin resistance in Listeria monocytogenes ATCC 700302 is a complex phenotype. Appl Environ Microbiol 64, 231–237.
    [Google Scholar]
  8. Dalet, K., Cenatiempo, Y., Cossart, P. & Héchard, Y. ( 2001; ). A σ 54-dependent PTS permease of the mannose family is responsible for sensitivity of Listeria monocytogenes to mesentericin Y105. Microbiology 147, 3263–3269.
    [Google Scholar]
  9. Dykes, G. A. & Hastings, J. W. ( 1998; ). Fitness costs associated with class IIa bacteriocin resistance in Listeria monocytogenes B73. Lett Appl Microbiol 26, 5–8.[CrossRef]
    [Google Scholar]
  10. Ennahar, S., Sashihara, T., Sonomoto, K. & Ishizaki, A. ( 2000; ). Class IIa bacteriocins, biosynthesis, structure and activity. FEMS Microbiol Rev 24, 85–106.[CrossRef]
    [Google Scholar]
  11. Fiedler, F., Seger, J., Schrettenbrunner, A. & Seeliger, H. ( 1984; ). The biochemistry of murein and cell wall teichoic acids in the genus Listeria. Syst Appl Microbiol 5, 360–376.[CrossRef]
    [Google Scholar]
  12. Fischer, W. & Leopold, K. ( 1999; ). Polar lipids of four listeria species containing l-lysylcardiolipin, a novel lipid structure, and other unique phospholipids. Int J Syst Bacteriol 49, 653–662.[CrossRef]
    [Google Scholar]
  13. Ganz, T. ( 2001; ). Fatal attraction evaded, how pathogenic bacteria resist polypeptides. J Exp Med 193, F31–F34.[CrossRef]
    [Google Scholar]
  14. Glaser, P., Frangeul, L., Buchrieser, C. & 54 other authors ( 2001; ). Comparative genomics of Listeria species. Science 294, 849–852.
    [Google Scholar]
  15. Gravesen, A., Warthoe, P., Knøchel, S. & Thirstrup, K. ( 2000; ). Restriction fragment differential display of pediocin-resistant Listeria monocytogenes 412 mutants shows consistent overexpression of a putative β-glucoside-specific PTS system. Microbiology 146, 1381–1389.
    [Google Scholar]
  16. Gravesen, A., Ramnath, M., Rechinger, B., Andersen, N., Jänsch, L., Héchard, Y., Hastings, J. W. & Knøchel, S. ( 2002; ). High-level resistance to class IIa bacteriocins is associated with one general mechanism in Listeria monocytogenes. Microbiology 148, 2361–2369.
    [Google Scholar]
  17. Gravesen, A., Kallipolitis, B., Holmstrøm, K., Høiby, P. E., Ramnath, M. & Knøchel, S. ( 2004; ). pbp 2229-mediated nisin resistance mechanism in Listeria monocytgenes confers cross-protection to class IIa bacteriocins and affects virulence gene expression. Appl Environ Microbiol 70, 1669–1679.[CrossRef]
    [Google Scholar]
  18. Hastings, J. W., Sailer, M., Johnson, K., Roy, K. L., Vederas, J. C. & Stiles, M. E. ( 1991; ). Characterization of leucocin A-UAL 187 and cloning of the gene from Leuconostoc gelidum. J Bacteriol 173, 7497–7500.
    [Google Scholar]
  19. Héchard, Y., Derijard, B., Letellierand, F. & Cenatiempo, Y. ( 1992; ). Characterization and purification of mesentericin Y105, an anti-Listeria bacteriocin from Leuconsotoc mesenteroides. J Gen Microbiol 138, 2725–2731.[CrossRef]
    [Google Scholar]
  20. Héchard, Y. & Sahl, H.-G. ( 2002; ). Mode of action of modified and unmodified bacteriocins from Gram-positive bacteria. Biochimie 84, 545–557.[CrossRef]
    [Google Scholar]
  21. Hsu, S.-T., Breukink, E., Bierbaum, G., Sahl, H.-G., De Kruijff, B., Kaptein, R., Van Nuland, N. A. J. & Bonvin, A. M. J. J. ( 2003; ). NMR study of mersacidin and lipid II interaction in DPC micelle: conformational changes are a key to antimicrobial activity. J Biol Chem 278, 13110–13117.[CrossRef]
    [Google Scholar]
  22. Kaya, S., Araki, Y. & Ito, E. ( 1985; ). Characterization of a novel linkage unit between ribitol teichoic acid and peptidoglycan in Listeria monocytogenes cell wall. Eur J Biochem 146, 517–522.[CrossRef]
    [Google Scholar]
  23. Klaenhammer, T. ( 1993; ). Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev 12, 39–86.[CrossRef]
    [Google Scholar]
  24. Maisnier-Patin, S. & Richard, J. ( 1996; ). Cell wall changes in nisin-resistant variants of Listeria innocua grown in the presence of high nisin concentrations. FEMS Microbiol Lett 140, 29–35.[CrossRef]
    [Google Scholar]
  25. Mantovani, H. & Russell, J. ( 2001; ). Nisin resistance of Streptococcus bovis. Appl Environ Microbiol 67, 808–813.[CrossRef]
    [Google Scholar]
  26. Montville, T. J. & Chen, Y. ( 1998; ). Mechanistic action of pediocin and nisin: recent progress and unresolved questions. Appl Microbiol Biotechnol 50, 511–519.[CrossRef]
    [Google Scholar]
  27. Peschel, A. & Collins, L. ( 2001; ). Staphylococcal resistance to antimicrobial peptides of mammalian and bacterial origin. Peptides 22, 1651–1659.[CrossRef]
    [Google Scholar]
  28. Peschel, A., Otto, M., Jack, R., Kalbacher, H., Jung, G. & Götz, F. ( 1999; ). Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274, 8405–8410.[CrossRef]
    [Google Scholar]
  29. Peschel, A., Vuong, C., Otto, M. & Götz, F. ( 2000; ). The d-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antimicrob Agents Chemother 44, 2845–2847.[CrossRef]
    [Google Scholar]
  30. Peschel, A., Jack, R., Otto, M. & 9 other authors ( 2001; ). Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with l-lysine. J Exp Med 193, 1067–1076.[CrossRef]
    [Google Scholar]
  31. Peteroy, M., Severin, A., Zhao, F. & 8 other authors ( 2000; ). Characterization of a Mycobacterium smegmatis mutant that is simultaneously resistant to d-cycloserine and vancomycin. Antimicrob Agents Chemother 44, 1701–1704.[CrossRef]
    [Google Scholar]
  32. Quadri, L. E. N., Sailer, M., Roy, K. L., Vederas, J. C. & Stiles, M. E. ( 1994; ). Chemical and genetic characterization of bacteriocins produced by Carnobacterium piscicola LV17B. J Biol Chem 269, 12204–12211.
    [Google Scholar]
  33. Ramnath, M., Beukes, M., Tamura, K. & Hastings, J. W. ( 2000; ). Absence of a putative mannose-specific phosphotransferase system enzyme IIAB component in a leucocin A-resistant strain of Listeria monocytogenes, as shown by two-dimensional sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Appl Environ Microbiol 66, 3098–3101.[CrossRef]
    [Google Scholar]
  34. Scott, M., Gold, M. & Hancock, R. E. W. ( 1999; ). Interaction of cationic peptides with lipoteichoic acid and Gram-positive bacteria. Infect Immun 67, 6445–6453.
    [Google Scholar]
  35. Thompson, T., Bouwer, H., Portnoy, D. & Frankel, F. ( 1998; ). Pathogenicity and immunogenicity of a Listeria monocytogenes strain that requires d-alanine for growth. Infect Immun 66, 3552–3561.
    [Google Scholar]
  36. Vadyvaloo, V., Hastings, J. W., Van der Merwe, M. & Rautenbach, M. ( 2002; ). Membranes of class IIa bacteriocin-resistant Listeria monocytogenes cells contain increased levels of desaturated and short-acyl-chain phosphatidylglycerols. Appl Environ Microbiol 68, 5223–5230.[CrossRef]
    [Google Scholar]
  37. Vadyvaloo, V., Snoep, J. L., Hastings, J. W. & Rautenbach, M. ( 2004; ). Physiological implications of class IIa bacteriocin resistance in Listeria monocytogenes strains. Microbiology 150, 335–340.[CrossRef]
    [Google Scholar]
  38. Wargel, R., Shadur, C. & Neuhaus, F. ( 1971; ). Mechanism of d-cycloserine action, transport mutants for d-alanine, d-cycloserine, and glycine. J Bacteriol 105, 1028–1035.
    [Google Scholar]
  39. Webster, J., Bannerman, T., Hubner, R., Ballard, D., Cole, E., Bruce, J., Fiedler, F., Schubert, K. & Kloos, W. ( 1994; ). Identification of the Staphylococcus sciuri species group with EcoRI fragments containing rRNA sequences and description of Staphylococcus vitulus sp. nov. Int J Syst Bacteriol 44, 454–460.[CrossRef]
    [Google Scholar]
  40. Yan, L. Z., Gibbs, A. C., Stiles, M. E., Wishart, D. S. & Vederas, J. C. ( 2000; ). Analogues of bacteriocins, antimicrobial specificity and interactions of leucocin A with its enantiomer, carnobacteriocin B2 and truncated derivatives. J Med Chem 43, 4579–4581.[CrossRef]
    [Google Scholar]
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