Cheddar cheese cooking temperature induces differential lactococcal cell permeabilization and autolytic responses as detected by flow cytometry: Implications for intracellular enzyme accessibility

Journal of Applied Microbiology

Volumn 99, Issue 5, 2005, Pages 1007-1018

  Sheehan, A ^a   O'Loughlin, C ^b   O'Cuinn, G ^c   FitzGerald, R J ^b   Wilkinson, Martin G ^b,c  

^a ANIMAL AND GRASSLAND RESEARCH AND INNOVATION CENTRE   (Ireland)

^b Atlantic Technological University Sligo   (Ireland)

^c UNIVERSITY OF LIMERICK   (Ireland)

Author keywords

Autolysis; Enzymes; Flow cytometry; Lactococci; Permeabilization

Indexed keywords

CELL CULTURE; CELL PROLIFERATION; ENZYME ACTIVITY; FLOW CYTOMETRY; LACTIC ACID; STARTERS;

AUTOLYSIS; CHEDDAR CHEESE; CHEESE JUICE; COOKING TEMPERATURES; ENZYME ACCESSIBILITY; ENZYMES ACTIVITY; INTRACELLULAR ENZYME; LACTOCOCCUS; PERMEABILIZATION; PERMEABILIZED CELLS;

STRAIN;

LACTATE DEHYDROGENASE;

ENZYME ACTIVITY;

ARTICLE; AUTOLYSIS; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIUM CULTURE; CELL MEMBRANE PERMEABILITY; CHEESEMAKING; COOKING; ENZYME ASSAY; FLOW CYTOMETRY; FLUORESCENCE; LACTIC ACID BACTERIUM; LACTOCOCCUS; NONHUMAN; PLATE COUNT; TEMPERATURE;

BACTERIA (MICROORGANISMS); LACTOCOCCI; LACTOCOCCUS; LACTOCOCCUS LACTIS;

EID: 27444438006     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2005.02718.x     Document Type: Article

References (35)

1. Booth, M., Donnelly, W.J., Ni Fhaolain, I., Jennings, P.V. and O'Cuinn, G. (1990) Proline-specific peptidases of Streptococcus cremoris AM2. J Dairy Res 57, 79-88.
2. Buist, G., Venema, G. and Kok, J. (1998) Autolysis of Lactococcus lactis is influenced by proteolysis. J Bacteriol 180, 5947-5953.
3. Bunthof, C.J., van Schalkwijk, S., Meijer, W., Abee, T. and Hugenholtz, J. (2001) Fluorescent method for monitoring starter permeabilization and lysis. Appl Environ Microbiol 67, 4264-4271.
4. Chapot-Chartier, M.P., Deniel, C., Rousseau, M., Vassal, L. and Gripon, J.C. (1994) Autolysis of two strains of Lactococcus lactis during cheese ripening. Int Dairy J 4, 251-269.
5. Collins, Y.F., Mc Sweeney, P.L.H. and Wilkinson, M.G. (2003) Evidence for a relationship between autolysis of starter bacteria and lipolysis in Cheddar cheese. J Dairy Res 70, 105-113.
6. Crow, V.L., Coolbear, T., Gopal, P.K., Martley, F.G., McKay, L.L. and Reipe, H. (1995) The role of autolysis of lactic acid bacteria in the ripening of cheese. Int Dairy J 5, 855-875.
7. Feirtag, J.M. and McKay, L.L. (1987) Thermoinducible lysis of temperature-sensitive Streptococcus cremoris strains. J Dairy Sci 70, 1779-1784.
8. Fox, P. F. and Wallace, J.M. (1997) Formation of flavour compounds in cheese. Adv Appl Microbiol 45, 17-85.
9. Gagnaire, V., Lortal, S. and Leonil, J. (1998) Free active peptidases are detected in Emmental juice extracted before ripening in the warm room. J Dairy Res 65, 119-128.
10. International Dairy Federation (1979) Cheese and Processed Products. Determination of Chloride Content. Potentiometric Titration Method. Brussels: IDF (FIL-IDF Standard no. 88).
11. International Dairy Federation (1982) Cheese and Processed Products. Determination of the Total Solids Content (Reference Method). Brussels: IDF (FIL-IDF Standard no. 4).
12. International Dairy Federation (1986a) Cheese and Processed Products. Determination of Nitrogen Content (Kjeldahl Method) and Calculation of Crude Protein Content. Brussels: IDF (FIL-IDF Standard no. 20A).
13. International Dairy Federation (1986b) Cheese and Processed Products. Determination of Fat Content. Gravimetric Method. Brussels: IDF (FIL-IDF Standard no. 127).
14. Kato, T., Nagatsu, T., Kimura, T. and Sakakibara, S. (1978) Fluorescence assay of X-prolyl dipeptidyl-aminopeptidase activity with a new fluorogenic substrate. Biochem Med 19, 351-359.
15. Laan, H., Tan, S.E., Bruinenberg, P., Limsowtin, G. and Broome, M. (1998) Aminopeptidase activities of starter and non-starter lactic acid bacteria under simulated Cheddar cheese ripening conditions. Int Dairy J 8, 267-274.
16. Lepeuple, A.S., Vassal, L., Cesselin, B., Delacroix-Buchet, A., Gripon, J.-C. and Chapot-Chartier, M.P. (1998) Involvement of a prophage in the lysis of Lactococcus lactis subsp. cremoris AM2 during cheese ripening. Int Dairy J 8, 667-674.
17. Lowrie, R.J., Lawrence, R.C. and Pearce, L.E. (1972) Cheddar cheese flavour. III. The growth of lactic streptococci during cheese making and the effect on bitterness development. N Z J Dairy Sci Technol 7, 44-50.
18. Lowrie, R.J., Lawrence, R.C. and Peberdy, M.F. (1974) Cheddar cheese flavour. V. Influence of bacteriophage and cooking temperature on cheese made under controlled bacteriological conditions. N Z J Dairy Sci Technol 9, 116-121.
19. Martley, F.G. and Lawrence, R.C. (1972) Cheddar cheese flavour: II. Characteristics of single strain starters associated with good or poor flavour development. N Z J Dairy Sci Technol 7, 38-44.
20. Meijer, W., Dobbelaar, C. and Hugenholtz, J. (1998) Thermoinducible lysis in Lactococcus lactis subsp. cremoris SK11: implications for cheese ripening. Int Dairy J 8, 275-280.
21. Morgan, S., O'Donovan, C., Ross, R.P., Hill, C. and Fox, P.F. (1995) Significance of autolysis and bacteriocin-induced lysis of starter cultures in Cheddar cheese ripening. In Proceedings of the 4th Cheese Symposium, pp. 51-60. Moorepark and Cork: Teagasc and University College Cork.
22. Morris, H.A., Holt, C., Brooker, B.E., Banks, J.M. and Manson, W. (1988) Inorganic constituents of cheese: analysis of juice from a one-month old Cheddar cheese and the use of light and electron microscopy to characterise the crystalline phases. J Dairy Res 55, 255-268.
23. Niven, G.W. and Mulholland, F. (1998) Cell membrane integrity and lysis in Lactococcus lactis: the detection of a population of permeable cells in post-logarithmic phase cultures. J Appl Microbiol 84, 90-96.
24. O'Donovan, C.M., Wilkinson, M.G., Guinee, T.P. and Fox, P.F. (1996) An investigation of the autolytic properties of three lactococcal strains during cheese ripening. Int Dairy J 6, 1149-1165.
25. O'Reilly, C.E., O'Conner, P.M., Murphy, P.M., Kelly, A.L. and Beresford, T.P. (2002) Effects of high-pressure treatment on autolysis of starter bacteria and proteolysis in Cheddar cheese. Int Dairy J 12, 915-922.
26. O'Sullivan, D., Ross, R.P., Fitzgerald, G.F. and Coffey, A. (2000) Investigation of the relationship between lysogeny and lysis of Lactococcus lactis in cheese using prophage-targeted PCR. Appl Environ Microbiol 66, 2192-2198.
27. Rogosa, M., Mitchell, J.A. and Wiseman, R.F. (1951) A selective medium for isolation and enumeration of oral and faecal lactobacilli. J Bacteriol 62, 132-133.
28. Salvat-Brunaud, D., Maubois, J.L., Le Graët, Y., Piot, M., Maillard, M.B., Corre, C. and Thierry, A. (1995) Extraction and composition of the aqueous phase of Emmental during ripening. Lait 75, 239-249.
29. Stuart, M.R., Chou, L.S. and Weimer, B.C. (1999) Influence of carbohydrate starvation and arginine on culturability and amino acid utilization of Lactococcus lactis subsp. lactis. Appl Environ Microbiol 65, 665-673.
30. Terzaghi, B.E. and Sandine, W.E. (1975) Improved medium for lactic streptococci and their bacteriophages. Appl Microbiol 29, 807-813.
31. Wilkinson, M.G., Guinee, T.P. and Fox, P.F. (1994a) Factors which may influence the determination of autolysis of starter bacteria during Cheddar cheese ripening. Int Dairy J 4, 141-160.
32. Wilkinson, M.G., Guinee, T.P., O'Callaghan, D.M. and Fox, P.F. (1994b) Autolysis and proteolysis in different strains of starter bacteria during Cheddar cheese ripening. J Dairy Res 61, 249-262.
33. Wilkinson, M.G., Guinee, T.P., O'Callaghan, D.M. and Fox, P.F. (1995) Effect of cooking temperature on the autolysis of starter, Lactococcus lactis subsp. cremoris AM2, and the maturation of Cheddar cheese. Milchwissenschaft 50, 376-380.
34. Wittenberger, C.L. and Angelo, N. (1970) Purification and properties of a fructose-1,6-diphosphate-activated lactate dehydrogenase from Streptococcus faecalis. J Bacteriol 101, 717-724.
35. Wong, H.C. and Wang, P. (2004) Induction of viable but nonculturable state in Vibrio parahaemolyticus and its susceptibility to environmental stresses. J Appl Microbiol 96, 359-366.