Complex phenotypic and genotypic responses of Listeria monocytogenes strains exposed to the class IIa bacteriocin sakacin P

Applied and Environmental Microbiology

Volumn 75, Issue 22, 2009, Pages 6973-6980

  Tessema, Girum Tadesse ^a,b   Møretrø, Trond ^a   Kohler, Achim ^a,b   Axelsson, Lars ^a   Naterstad, Kristine ^a  

^a NOFIMA   (Norway)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

DISEASES; FATTY ACIDS; FOURIER TRANSFORM INFRARED SPECTROSCOPY; GENE ENCODING;

ACQUIRED RESISTANCE; BACTERIOCIN RESISTANCE; FOOD-BORNE PATHOGENS; GENETIC CHARACTERISTICS; INHIBITORY CONCENTRATION; LISTERIA MONOCYTOGENES; RESISTANCE MECHANISMS; SUBSTANTIAL VARIATIONS;

LISTERIA;

BACTERIOCIN; PHOSPHOTRANSFERASE; SAKACIN P; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOFILM; FOOD PROCESSING; GENE EXPRESSION; INHIBITOR; PHYSIOLOGICAL RESPONSE; POLYSACCHARIDE; PROTEIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM MUTANT; BIOFILM; CARBON SOURCE; CONTROLLED STUDY; DOWN REGULATION; EXPOSURE; GENE EXPRESSION REGULATION; GENETIC CODE; GENOTYPE; IC 50; LISTERIA MONOCYTOGENES; MICROBIAL DIVERSITY; NONHUMAN; OPERON; PHENOTYPIC VARIATION; STRESS; UPREGULATION; WILD TYPE;

LISTERIA MONOCYTOGENES;

EID: 70449408699     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00608-09     Document Type: Article

References (49)

1. Glc in regulation of energy metabolism, biofilm development, and competence in Streptococcus mutans. J. Bacteriol. 188:3748-3756.
2. Arous, S., K. Dalet, and Y. Hechard. 2004. Involvement of the mpo operon in resistance to class IIa bacteriocins in Listeria monocytogenes. FEMS Microbiol. Lett. 238:37-41.
3. Barabote, R. D., and M. H. Saier, Jr. 2005. Comparative genomic analyses of the bacterial phosphotransferase system. Microbiol. Mol. Biol. Rev. 69:608-634.
4. Borucki, M. K., J. D. Peppin, D. White, F. Loge, and D. R. Call. 2003. Variation in biofilm formation among strains of Listeria monocytogenes. Appl. Environ. Microbiol. 69:7336-7342.
5. Cotter, P. D., C. Hill, and R. P. Ross. 2005. Bacteriocins: developing innate immunity for food. Nat. Rev. Microbiol. 3:777-788.
6. 54-dependent PTS operon of the lactose family in Listeria monocytogenes. Biochimie 85:633-638.
7. 54-dependent PTS permease of the mannose family is responsible for sensitivity of Listeria monocytogenes to mesentericin Y105. Microbiology 147:3263-3269.
8. Diep, D. B., M. Skaugen, Z. Salehian, H. Holo, and I. F. Nes. 2007. Common mechanisms of target cell recognition and immunity for class II bacteriocins. Proc. Natl. Acad. Sci. USA 104:2384-2389.
9. Drider, D., G. Fimland, Y. Hechard, L. M. McMullen, and H. Prevost. 2006. The continuing story of class IIa bacteriocins. Microbiol. Mol. Biol. Rev. 70:564-582.
10. Duffes, F., P. Jenoe, and P. Boyaval. 2000. Use of two-dimensional electrophoresis to study differential protein expression in divercin V41-resistant and wild-type strains of Listeria monocytogenes. Appl. Environ. Microbiol. 66: 4318-4324. (Pubitemid 30768524)
11. Dykes, G. A., and J. W. Hastings. 1998. Fitness costs associated with class IIa bacteriocin resistance in Listeria monocytogenes B73. Lett. Appl. Microbiol. 26:5-8.
12. Eijsink, V. G. H., L. Axelsson, D. B. Diep, L. S. Håvarstein, H. Holo, and I. F. Nes. 2002. Production of class II bacteriocins by lactic acid bacteria; an example of biological warfare and communication. Antonie van Leeuwenhoek 81:639-654.
13. Eijsink, V. G. H., M. Skeie, P. H. Middelhoven, M. B. Brurberg, and I. F. Nes. 1998. Comparative studies of class IIa bacteriocins of lactic acid bacteria. Appl. Environ. Microbiol. 64:3275-3281.
14. Ennahar, S., N. Deschamps, and J. Richard. 2000. Natural variation in susceptibility of Listeria strains to class IIa bacteriocins. Curr. Microbiol. 41:1-4.
15. Ennahar, S., T. Sashihara, K. Sonomoto, and A. Ishizaki. 2000. Class IIa bacteriocins: biosynthesis, structure and activity. FEMS Microbiol. Rev. 24: 85-106.
16. Gandhi, M., and M. L. Chikindas. 2007. Listeria: A foodborne pathogen that knows how to survive. Int. J. Food Microbiol. 113:1-15.
17. Giotis, E. S., I. S. Blair, and D. A. McDowell. 2007. Morphological changes in Listeria monocytogenes subjected to sublethal alkaline stress. Int. J. Food Microbiol. 120:250-258.
18. Glaser, P., L. Frangeul, C. Buchrieser, C. Rusniok, A. Amend, F. Baquero, P. Berche, H. Bloecker, P. Brandt, T. Chakraborty, A. Charbit, F. Chetouani, E. Couve, A. de Daruvar, P. Dehoux, E. Domann, G. Dominguez-Bernal, E. Duchaud, L. Durant, O. Dussurget, K.-D. Entian, H. Fsihi, F. G.-D. Portillo, P. Garrido, L. Gautier, W. Goebel, N. Gomez-Lopez, T. Hain, J. Hauf, D. Jackson, L.-M. Jones, U. Kaerst, J. Kreft, M. Kuhn, F. Kunst, G. Kurapkat, E. Madueno, A. Maitournam, J. M. Vicente, E. Ng, H. Nedjari, G. Nordsiek, S. Novella, B. de Pablos, J.-C. Perez-Diaz, R. Purcell, B. Remmel, M. Rose, T. Schlueter, N. Simoes, A. Tierrez, J.-A. Vazquez-Boland, H. Voss, J. Wehland, and P. Cossart. 2001. Comparative genomics of Listeria species. Science 294:849-852.
19. Gravesen, A., A.-M. Jydegaard Axelsen, J. Mendes da Silva, T. B. Hansen, and S. Knochel. 2002. Frequency of bacteriocin resistance development and associated fitness costs in Listeria monocytogenes. Appl. Environ. Microbiol. 68:756-764.
20. Gravesen, A., B. Kallipolitis, K. Holmstrom, P. E. Hoiby, M. Ramnath, and S. Knochel. 2004. pbp2229-mediated nisin resistance mechanism in Listeria monocytogenes confers cross-protection to class IIa bacteriocins and affects virulence gene expression. Appl. Environ. Microbiol. 70:1669-1679.
21. Gravesen, A., M. Ramnath, K. B. Rechinger, N. Andersen, L. Jansch, Y. Hechard, J. W. Hastings, and S. Knochel. 2002. High-level resistance to class IIa bacteriocins is associated with one general mechanism in Listeria monocytogenes. Microbiology 148:2361-2369.
22. Holck, A. L., L. Axelsson, K. Hühne, and L. Kröckel. 1994. Purification and cloning of sakacin 674, a bacteriocin from Lactobacillus sake Lb674. FEMS Microbiol. Lett. 115:143-150.
23. Katla, T., T. Moretro, I. Sveen, I. M. Aasen, L. Axelsson, L. M. Rorvik, and K. Naterstad. 2002. Inhibition of Listeria monocytogenes in chicken cold cuts by addition of sakacin P and sakacin P-producing Lactobacillus sakei. J. Appl. Microbiol. 93:191-196. (Pubitemid 34989136)
24. Katla, T., T. Moretro, I. M. Aasen, A. Holck, L. Axelsson, and K. Naterstad. 2001. Inhibition of Listeria monocytogenes in cold smoked salmon by addition of sakacin P and/or live Lactobacillus sakei cultures. Food Microbiol. 18:431-439.
25. Katla, T., K. Naterstad, M. Vancanneyt, J. Swings, and L. Axelsson. 2003. Differences in susceptibility of Listeria monocytogenes strains to sakacin P, sakacin A, pediocin PA-1, and nisin. Appl. Environ. Microbiol. 69:4431-4437.
26. Klaenhammer, T. R. 1993. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Rev. 12:39-86.
27. Kohler, A., U. Böcker, J. Warringer, A. Blomberg, S. Omholt, E. Stark, and H. Martens. 2009. Reducing inter-replicate variation in Fourier-transform infrared spectroscopy by extended multiplicative signal correction. Appl. Spectrosc. 63:296-305.
28. Lianou, A., J. D. Stopforth, Y. Yoon, M. Wiedmann, and J. N. Sofos. 2006. Growth and stress resistance variation in culture broth among Listeria monocytogenes strains of various serotypes and origins. J. Food Prot. 69:2640-2647.
29. Lunden, J., R. Tolvanen, and H. Korkeala. 2004. Human listeriosis outbreaks linked to dairy products in Europe. J. Dairy Sci. 87:E6-E12.
30. Mead, P. S., L. Slutsker, V. Dietz, L. F. McCaig, J. S. Bresee, C. Shapiro, P. M. Griffin, and R. V. Tauxe. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607-625.
31. Medircio, S. N., V. A. Leao, and M. C. Teixeira. 2007. Specific growth rate of sulfate reducing bacteria in the presence of manganese and cadmium. J. Hazard. Mater. 143:593-596.
32. Moretro, T., K. Naterstad, E. Wang, I. M. Aasen, S. Chaillou, M. Zagorec, and L. Axelsson. 2005. Sakacin P non-producing Lactobacillus sakei strains contain homologues of the sakacin P gene cluster. Res. Microbiol. 156:949-960.
33. Naghmouchi, K., E. Kheadr, C. Lacroix, and I. Fliss. 2007. Class I/class IIa bacteriocin cross-resistance phenomenon in Listeria monocytogenes. Food Microbiol. 24:718-727.
34. Naumann, D. 2000. Infrared spectroscopy in microbiology, p. 102-131. In R. A. Meyers (ed.), Encyclopedia of analytical chemistry. John Wiley & Sons, Ltd., Chichester, United Kingdom.
35. Oust, A., T. Moretro, K. Naterstad, G. D. Sockalingum, I. Adt, M. Manfait, and A. Kohler. 2006. Fourier transform infrared and Raman spectroscopy for characterization of Listeria monocytogenes strains. Appl. Environ. Microbiol. 72:228-232.
36. Ramnath, M., M. Beukes, K. Tamura, and J. W. Hastings. 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.
37. Rasch, M., and S. Knochel. 1998. Variations in tolerance of Listeria monocytogenes to nisin, pediocin PA-1 and bavaricin A. Lett. Appl. Microbiol. 27:275-278.
38. Rekhif, N., A. Atrih, and G. Lefebvre. 1994. Selection and properties of spontaneous mutants of Listeria monocytogenes ATCC 15313 resistant to different bacteriocins produced by lactic acid bacteria strains. Curr. Microbiol. 28:237-241.
39. 54) gene from Listeria monocytogenes is involved in resistance to mesentericin Y105, an antibacterial peptide from Leuconostoc mesenteroides. J. Bacteriol. 179:7591-7594.
40. Rode, T. M., S. Langsrud, A. Holck, and T. Møretrø. 2007. Different patterns of biofilm formation in Staphylococcus aureus under food-related stress conditions. Int. J. Food Microbiol. 116:372-383.
41. Schmittgen, T. D., and K. J. Livak. 2008. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3:1101-1108.
42. Tichaczek, P. S., J. Nissen-Meyer, I. F. Nes, R. F. Vogel, and W. P. Hammes. 1992. Characterization of the bacteriocins curvacin A from Lactobacillus curvatus LTH1174 and sakacin P from L. sake LTH673. Syst. Appl. Microbiol. 15:460-468.
43. Tichaczek, P. S., R. F. Vogel, and W. P. Hammes. 1994. Cloning and sequencing of sakP encoding sakacin P, the bacteriocin produced by Lactobacillus sake LTH673. Microbiology 140:361-367.
44. Vadyvaloo, V., S. Arous, A. Gravesen, Y. Hechard, R. Chauhan-Haubrock, J. W. Hastings, and M. Rautenbach. 2004. Cell-surface alterations in class IIa bacteriocin-resistant Listeria monocytogenes strains. Microbiology 150: 3025-3033.
45. Vadyvaloo, V., J. W. Hastings, M. J. van der Merwe, and M. Rautenbach. 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.
46. Vadyvaloo, V., J. L. Snoep, J. W. Hastings, and M. Rautenbach. 2004. Physiological implications of class IIa bacteriocin resistance in Listeria monocytogenes strains. Microbiology 150:335-340.
47. Vazquez-Boland, J. A., M. Kuhn, P. Berche, T. Chakraborty, G. Dominguez- Bernal, W. Goebel, B. Gonzalez-Zorn, J. Wehland, and J. Kreft. 2001. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 14:584-640.
48. Vignolo, G., J. Palacios, M. E. Farias, F. Sesma, U. Schillinger, W. Holzapfel, and G. Oliver. 2000. Combined effect of bacteriocins on the survival of various Listeria species in broth and meat system. Curr. Microbiol. 41:410-416.
49. Welshimer, H. J., and J. Donker-Voet. 1971. Listeria monocytogenes in nature. Appl. Environ. Microbiol. 21:516-519.