Two subpopulations of Listeria monocytogenes occur at subinhibitory concentrations of leucocin 4010 and nisin

Applied and Environmental Microbiology

Volumn 72, Issue 2, 2006, Pages 1631-1638

  Hornbæk, Tina ^a,b   Brockhoff, Per B ^a,c   Siegumfeldt, Henrik ^a   Budde, Birgitte Bjørn ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b CHR HANSEN A S   (Denmark)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; FLUORESCENCE; GENES; MICROSCOPIC EXAMINATION; PH EFFECTS; SODIUM COMPOUNDS;

FLUORESCENCE RATIO IMAGING MICROSCOPY (FRIM); LEUCOCIN 4010; LISTERIA MONOCYTOGENES; NISIN;

MICROBIOLOGY;

ACETIC ACID; BACTERIOCIN; CARBOXYFLUORESCEIN DIACETATE SUCCINIMIDYL ESTER; CITRATE SODIUM; LACTATE SODIUM; LEUCOCIN 4010; NISIN; SODIUM CHLORIDE; SODIUM DIHYDROGEN PHOSPHATE; SODIUM NITRITE; UNCLASSIFIED DRUG;

FOOD PROCESSING;

ANTIBACTERIAL ACTIVITY; ARTICLE; CELL SUBPOPULATION; CONTROLLED STUDY; DRUG INHIBITION; FLUORESCENCE RATIO IMAGING MICROSCOPY; FOOD PRESERVATION; IC 50; LISTERIA MONOCYTOGENES; MEAT; MICROSCOPY; NONHUMAN; PH; STAINING;

BACTERIOCINS; CELLS, IMMOBILIZED; FOOD MICROBIOLOGY; FOOD PRESERVATION; LISTERIA MONOCYTOGENES; MEAT; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; NISIN;

LISTERIA MONOCYTOGENES;

EID: 33144458802     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.72.2.1631-1638.2006     Document Type: Article

References (41)

1. Aasen, I. M., S. Markussen, T. Møretrø, T. Katla, L. Axelsson, and K. Naterstad. 2003. Interactions of the bacteriocins sakacin P and nisin with food constituents. Int. J. Food Microbiol. 87:35-43.
2. Abriouel, H., M. Maqueda, A. Gálvez, M. Martínez-Bueno, and E. Valdivia. Inhibition of bacterial growth, enterotoxin production, and spore outgrowth in strains of Bacillus cereus by bacteriocin AS-48. Appl. Environ. Microbiol. 68:1473-1477.
3. Attfield, P. V., H. Y. Choi, D. A. Veal, and P. J. L. Bell. 2001. Heterogeneity of stress gene expression and stress resistance among individual cells of Saccharomyces cerevisiae. Mol. Microbiol. 40:1000-1008.
4. Balaban, N. Q., J. Merrin, R. Chait, L. Kowalik, and S. Leibler. 2004. Bacterial persistence as a phenotypic switch. Science 305:1622-1625.
5. Barakat, R. K., and L. J. Harris. 1999. Growth of Listeria monocytogenes and Yersinia enterocolitica on cooked modified-atmosphere-packaged poultry in the presence and absence of a naturally occurring microbiota. Appl. Environ. Microbiol. 65:342-345.
6. Benkerroum, N., A. Daoudi, and M. Kamal. 2003. Behaviour of Listeria monocytogenes in raw sausages (merguez) in presence of a bacteriocin-producing lactococcal strain as a protective culture. Meat Sci. 63:479-484.
7. Bhunia, A. K., M. C. Johnson, and B. Ray. 1988. Purification, characterization, and antimicrobial spectrum of a bacteriocin produced by Pediococcus acidilactici. J. Appl. Bacteriol. 65:261-268.
8. Bhunia, A. K., M. C. Johnson, B. Ray, and N. Kalchayanand. 1991. Mode of action of pediocin AcH from Pediococcus acidilactici H on sensitive bacterial strains. J. Appl. Bacteriol. 70:25-33.
9. Budde, B. B., and M. Jakobsen. 2000. Real-time measurements of the interaction between single cells of Listeria monocytogenes and nisin on a solid surface. Appl. Environ. Microbiol. 66:3586-3591.
10. Budde, B., and M. Rasch. 2001. A comparative study on the use of flow cytometry and colony forming units for assessment of the antibacterial affect of bacteriocins. Int. J. Food Microbiol. 63:65-72.
11. Budde, B., T. Hornbæk, T. Jacobsen, V. Barkholt, and A. G. Koch. 2003. Leuconostoc camosum 4010 has the potential for the use as a protective culture for vacuum-packed meats: culture isolation, bacteriocin identification, and meat application experiments. Int. J. Food. Microbiol. 83:171-184.
12. Cameron, J. M. 1982. Error analysis, p. 515-545. In S. Kotz and N. L. Johnson (ed.), Encyclopedia of statistical science, vol. 2. John Wiley & Sons, Inc., New York, N.Y.
13. Choo-Smith, L.-P., K. Maquelin, T. van Vreeswijk, H. A. Bruning, G. J. Puppels, N. A. Ngo Thi, C. Kirschner, D. Naumann, D. Ami, A. M. Villa, F. Orsini, S. M. Doglia, H. Lamfarraj, G. D. Sockalingum, M. Manfait, P. Allouch, and H. P. Endtz. 2001. Investigating microbial (micro)colony heterogeneity by vibrational spectroscopy. Appl. Environ. Microbiol. 67:1461-1469.
14. Cole, M. B., M. V. Jones, and C. Holyoak. 1990. The effect of pH, salt concentration and temperature on the survival and growth of Listeria monocytogenes. Appl. Environ. Microbiol. 69:63-72.
15. Davey, H. M., and D. B. Kell. 1996. Flow cytometry and cell sorting of heterogeneous microbial populations: the importance of single-cell analysis. Microbiol. Rev. 60:641-696.
16. De Martinis, E. C. P., and B. D. G. M. Franco. 1998. Inhibition of Listeria monocytogenes in a pork product by a Lactobacillus sake strain. Int. J. Food Microbiol. 42:119-126.
17. De Martinis, E. C. P., and F. Z. Freitag. 2003. Screening of lactic acid bacteria from Brazilian meats for bacteriocin formation. Food Control 14: 197-200.
18. Dicks, L. M. T., F. D. Mellett, and L. C. Hoffman. 2004. Use of bacteriocin-producing starter cultures of Lactobacillus plantarum and Lactobacillus curvatus in production of ostrich meat salami. Meat Sci. 66:703-708.
19. Grau, F. H., and P. B. Vanderlinde. 1992. Occurrence, numbers, and growth of Listeria monocytogenes on some vacuum-packaged processed meats. J. Food Prot. 55:4-7.
20. Gravesen, A., A.-M. Jydegaard Axelsen, J. Mendes de Silva, T. B. Hansen, and S. Knøchel. 2002. Frequency of bacteriocin resistance development and associated fitness costs in Listeria monocytogenes. Appl. Environ. Microbiol. 68:756-764.
21. Guldfeldt, L. U., and N. Arneborg. 1998. Measurement of the effects of acetic acid and extracellular pH on intracellular pH of nonfermenting, individual Saccharomyces cerevisiae cells by fluorescence microscopy. Appl. Environ. Microbiol. 64:530-534.
22. Halm, M., T. Hornbæk, N. Arneborg, S. Sefa-Dedeh, and L. Jespersen. 2004. Lactic acid tolerance determined by measurement of intracellular pH of single cells of Candida krusei and Saccharomyces cerevisiae isolated from fermented maize dough. Int. J. Food Microbiol. 94:97-103.
23. Hornbæk, T., J. Dynesen, and M. Jakobsen. 2002. Use of fluorescence ratio imaging microscopy and flow cytometry for estimation of cell vitality for Bacillus licheniformis. FEMS Microbiol. Lett. 215:261-265.
24. Hornbæk, T., T. F. Brocklehurst, and B. B. Budde. 2004. The antilisterial effect of Leuconostoc camosum 4010 in the presence of sodium chloride and sodium nitrite examined in a structured gelatin system. Int. J. Food Microbiol. 92:129-140.
25. Hugas, M., M. Garriga, M. Pascual, M. T. Aymerich, and J. M. Monfort. 2002. Enhancement of sakacin K activity against Listeria monocytogenes in fermented sausages with pepper or manganese as ingredients. Food Microbiol. 19:519-528.
26. Jack, R. W., J. Wan, J. Gordon, K. Harmark, B. E. Davidson, A. J. Hillier, R. E. Wettenhall, M. W. Hickey, and M. J. Coventry. 1996. Characterization of the chemical and antimicrobial properties of piscicolin 126, a bacteriocin produced by Camobacterium piscicola JG126. Appl. Environ. Microbiol. 62:2897-2903.
27. Jacobsen, T., B. B. Budde, and A. G. Koch. 2003. Application of Leuconostoc camosum for biopreservation of cooked meat products. J. Appl. Microbiol. 94:1-8.
28. Jydegaard, A.-M., A. Gravesen, and S. Knøchel. 2000. Growth condition-related response of Listeria monocytogenes 412 to bacteriocin inactivation. Lett. Appl. Microbiol. 31:68-72.
29. Lee, S., T. Iwata, and H. Oyagi. 1993. Effects of salts on conformational change of basic amphipathic peptides from β-structure to α-helix in the presence of phospholipid liposomes and their channel-forming ability. Biochem. Biophys. Acta 1151:75-82.
30. Malakar, P. K., T. F. Brocklehurst, A. R. Mackie, P. D. G. Wilson, M. H. Zwietering, and K. van't Riet. 2000. Microgradients in bacterial colonies: use of fluorescence ratio imaging, a non-invasive technique. Int. J. Food Microbiol. 56:71-80.
31. Mattila, K., P. Saris, and S. Työppönen. 2003. Survival of Listeria monocytogenes on sliced cooked sausage after treatment with pediocin AcH. Int. J. Food Microbiol. 89:281-286.
32. McLachlan, G. J., and T. Krishnan. 1997. The EM-algorithm and extensions, p. 68-71. John Wiley & Sons, Inc., New York, N.Y.
33. Nykänen, A., K. Weckman, and A. Lapveteläinen. 2000. Synergistic inhibition of Listeria monocytogenes on cold-smoked rainbow trout by nisin and sodium lactate. Int. J. Food Microbiol. 61:63-72.
34. Parente, E., M. A. Giglio, A. Ricciardi, and C. Francesca. 1998. The combined effect of nisin, leucocin F10, pH, NaCl and EDTA on the survival of Listeria monocytogenes in broth. Int. J. Food Microbiol. 40:65-75.
35. Philips, C. A. 1999. The effect of citric acid, lactic acid, sodium citrate, and sodium lactate, alone and in combination with nisin, on the growth of Arcobacter butzleri. Lett. Appl. Microbiol. 29:424-428.
36. SAS Institute, Inc. 1999. SAS/STAT® user's guide, version 8, p. 1363-1464. SAS Institute, Inc., Cary, N.C.
37. Shabala, L., B. Budde, T. Ross, H. Siegumfeldt, and T. McMeekin. 2002. Responses of Listeria monocytogenes to acid stress and glucose availability monitored by measurements of intracellular pH and viable counts. Int. J. Food Microbiol. 75:89-97.
38. Siegumfeldt, H., K. B. Rechinger, and M. Jakobsen. 2000. Dynamic changes of intracellular pH in individual lactic acid bacterium cells in response to a rapid drop in extracellular pH. Appl. Environ. Microbiol. 66:2330-2335.
39. Sumner, E. R., and S. V. Avery. 2002. Phenotypic heterogeneity: differential stress resistance among individual cells of the yeast Saccharomyces cerevisiae. Microbiology 148:345-351.
40. van Laack, R. L. J. M., U. Schillinger, and W. H. Holzapfel. 1992. Characterization and partial purification of a bacteriocin produced by Leuconostoc camosum LA44A. Int. J. Food Microbiol. 16:183-195.
41. Vignolo, G., S. Fadda, M. N. de Kairuz, A. P. de, R. Holgado, and G. Oliver. 1998. Effects of curing additives on the control of Listeria monocytogenes by lactocin 705 in meat slurry. Food Microbiol. 15:259-264.