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http://dx.doi.org/10.5851/kosfa.2009.29.1.1

The Characteristics, Detection and Control of Bacteriophage in Fermented Dairy Products  

Ahn, Sung-Il (Department of Food Science and Technology, Sejong University)
Azzouny, Rehab A. (Department of Food Science and Technology, Sejong University)
Huyen, Tran Thi Thanh (Department of Civil and Environmental Engineering, Sejong University)
Kwak, Hae-Soo (Department of Food Science and Technology, Sejong University)
Publication Information
Food Science of Animal Resources / v.29, no.1, 2009 , pp. 1-14 More about this Journal
Abstract
This study was to review the classification, detection and control of bacteriophage in fermented dairy products. Bacteriophage has lytic and/or lysogenic life cycles. Epidemiologically speaking, detected major phages are c2, 936 and p335. Among them p335 has been the largest concern in dairy industry. Traditionally, various analytical technologies, such as spot, starter activity, indicator test, ATP measurement and conductimetric analysis, have been used for the phage detection. In recent years, advanced methods such as flow cytometric method, petrifilm, enzyme linked immunosorbent assay (ELISA) and multiflex PCR diagnostic kit have been deveoloped. The phage contamination has been controlled by using heat, high-pressure treatment, and the combinations of heat and pressure, and/or chemical. Also some starter cultures with phage-resistant character have been developed to minimize the concentration of phages in dairy product. Bacteriophage inhibition media such as calcium medium was also mentioned. To prevent the contamination of bacteriophage in dairy industry, further researches on the detection and control of phage, and phage resistant starters are necessary in the future.
Keywords
bacteriophage; classification; detection; control; dairy products;
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1 Azaiez, S. R. C., Fliss, I., Simard, R. E., and Moineau, S. (1998) Monoclonal antibodies raised against native major capsid proteins of lactococcal c2-like bacteriophages. Appl. Environ. Microbiol. 64, 4255-4259   PUBMED
2 Benbadis, L., Faelen, M., Slos, P., Fazel, A., and Mercenier, A. (1990) Characterization and comparison of virulent bacteriophages of Streptococcus thermophilus isolated from yoghurt. Biochimie 72, 855-862   DOI   PUBMED   ScienceOn
3 Brussow, H., Fremont, M., Bruttin, A., Sidoti, J., Constable, A., and Fryder, V. (1994) Detection and classification of Streptococcus thermophilus bacteriophages isolated from industrial milk fermentation. Appl. Environ. Microbiol. 60, 4537-4543   PUBMED
4 Brussow, H. and Bruttin, A. (1995) Characterization of a temperate Streptococcus thermophilus bacteriophage and its genetic relationship with lytic phages. Virology 212, 632–640   DOI   PUBMED   ScienceOn
5 Duplessis, M., Levesque, C. M., and Moineau, S. (2006). Characterization of Streptococcus thermophilus host range phage mutants. Appl. Environ. Microbiol. 72, 3036-3041   DOI   ScienceOn
6 Henning, D. R., Black, C. H., Sandine, W. E., and Elliker, P. R. (1986) Host range studies of lactic streptococcal bacteriophages. J. Dairy Sci. 51, 16-21   DOI
7 Jarvis, A. W., Fitzgerald, G. F., Mata, M., Mercenier, A., Neve, H., Powell, I. B., Ronda, C., Saxelin, M., and Teuber, M. (1991) Species and type phages of lactococcal bacteriophages. Intervirology 32, 2-9   PUBMED
8 Josephsen, J., Nyengaard, N. R., Vogensen, F. K., and Madesen, A. (1996) Plasmid-derived type II restriction-modification systems from Lactococcus lactis. PCT WO9625503
9 Klaenhammer, T. and Sanozky, R. (1989) pTN1060, a conjugal plasmid and derivatives thereof that confer phage resistance to group N streptococci. US Patent 4883756
10 Ledford, R. A. and Speck, M. L. (1979) Injury of lactic streptococci by culturing in media mechanisms high phosphates. J. Dairy Sci. 62, 781-784   DOI
11 McGrath, S., Fitzgerald, G. F., and Sinderen, D. V. (2004a) Cheese chemistry, physics and microbiology. 3th ed. Elsevier, Ltd.
12 Michelsen, O., Cuesta-Dominguez, A., Albrechtsen, B., and Jensen, P. R. (2007) Detection of bacteriophage-infected cells of Lactococcus lactis by using flow cytometry. Appl. Environ. Microbiol. 73, 7575-7581   DOI   ScienceOn
13 Robertson, P. (1993) Are phage-inhibitory media necessary? UW Dairy Pipeline 5, 1-11
14 McIntyre, K., Heap, H. A., Davey, G. P., and Limsowtin, G. K. Y. (1991) The distribution of lactococcal bacteriophage in the environment of cheese manufacturing plant. Int. Dairy J. 1, 183-197   DOI   ScienceOn
15 Suarez, V. B., Quiberoni, A., Binetti, A. G., and Reinheimer, J. A. (2002) Thermophilic lactic acid bacteria phages isolated from Argentinian dairy industries. J. Food Prot. 65, 1597-1604   PUBMED
16 Szcepanska, A. K., Hejnowicz, M. S., Kolakowski, P., and Barcowski, J. (2007) Biodiversity of Lactococcus lactis bacteriophages in Polish dairy environ. Acta Polonica 54,151-158   PUBMED
17 Whithead, R. H. (1953) Bacteriophage in cheese manufacture. J. Dairy Sci. 17, 109-123
18 Mata, M. and Ritzenthaler, P. (1988) Present state of lactic acid bacteria phage taxonomy. Biochimie 70, 395-399   DOI   ScienceOn
19 Binetti, A. G., Beatriz, D. R., Martin, M. C., and Alvarez, M. A. (2005) Detection and characterization of Streptococcus thermophilus bacteriophages by use of antireceptor gene sequence. Appl. Environ. Microbiol. 71, 6096-6103   DOI   ScienceOn
20 Buzrul, S., $\ddot{O}$zturkb, P., Alpa, H., and Akcelik, M. (2007) Thermal and chemical inactivation of lactococcal bacteriophages. LWT-Food Sci. Technol. 40, 1671-1677   DOI   ScienceOn
21 Lopez-Fandino, R., Carrascosa, A. V., and Olano, A. (1996) The effects of high pressure on whey protein denaturation and cheese-making properties of raw milk. J. Dairy Sci. 79, 929-936   DOI   ScienceOn
22 Sinkoff, B. A. and Bundus, R. H. (1983) Bulk starter media. US Patent 4,402,986
23 Quiberoni, A., Auad, L., Binetti, A. G., Sua'rez, V. B., Reinheimer, J. A., and Raya, R. R. (2003) Comparative analysis of Streptococcus thermophilus bacteriophages isolated from a yogurt industrial plant. Food Microbiol. 20, 461–469   DOI   ScienceOn
24 Dupont, K., Vogensen, F. K., and Josephsen, J. (2005) Detection of lactococcal 936-species bacteriophages in whey by magnetic capture hybridization PCR targeting a variable region of receptor-binding protein genes. J. Appl. Microbiol. 98, 1001-1009   DOI   ScienceOn
25 Moineau, S., Emond, E., Walker, S. A., Vedamuthu, E. R., and Kondo, J. K. (1999) DNA encoding phage resistance protein. US Patent 05994118
26 Powell, I. B., Arnold, P. M., Hillier, A. J., and Davidson, B. E. (1989) Molecular comparison of prolate-and isometricheaded bacteriophages of lactococci. Can. J. Microbiol. 35, 860-866   DOI
27 Bissonnette, F., Labrie, S., Deveau, H., Lmaoureux, M., and Moineau, S. (2000) Characterization of mesophilic mixed starter cultures used for the manufacture of aged Cheddar cheese. J. Dairy Sci. 83, 620-627   DOI   ScienceOn
28 Champagne, C. P. Piette, M., and Saint-Gelais, D. (1995) Characteristics of lactococcal cultures produced in commercial media. J. Ind. Microbiol. 15, 472-479   DOI   ScienceOn
29 Campbell, N. A. and Reece, J. B. (2001). Biology. 6th ed. Benjamin Cummings Press
30 Gaudreau, H., Fliss, I., and Champagne, C. P. (2006) Stability of autolytic lactococci during starter production and storage in commercial whey-based media. Int. Dairy J. 16, 200-206   DOI   ScienceOn
31 Moineau S., Bouchard J., and Dion. L. (2006) Fragment of Lactococcus lactis plasmid conferring antiphage activity and uses thereof. US Patent 7119167B2
32 Tseng, Y. C. and Hicks, C. L. (2008) Simplified petrifilm assay for lactococcus phage. Abstract W76 ADSA-ASAS Annual Meeting, pp. 217-218
33 Bush, M. L. (2002) Method of inhibiting bacteriophage infections in lactococcal bacteria. Abstract 1637 ADSAASAS Annual Meeting, p. 408
34 Del Rio B., Binetti, A. G., Martin, M. C., Fernandez, M., Magadan, A. H., and Alvarez, M. A. (2007) Multiplex PCR for the detection and identification of dairy bacteriophages in milk. Food Microbiol. 24, 75-81   DOI   ScienceOn
35 Madera, C., Monjardin, C., and Suarez, J. E. (2004) Milk contamination and resistance to processing conditions determine the fate of Lactococcus lactis bacteriophages in dairies. Appl. Environ. Microbiol. 70, 7365-7371   DOI   ScienceOn
36 Moineau, S., Fortier, J., Ackermann, H. W., and Pandian, S. (1992) Characterization of lactococcal bacteriophages from Quebec cheese plants. Can. J. Microbiol. 38, 875-882   DOI
37 Prescott, L., Harley, J., and Klein, D. (2002) Microbiology. 5th ed. Mcgraw Hill Publishing Co., pp. 348-361
38 Br$\ddot{u}$ssow, H. and Hendrix R. W. (2002) Phage genomics: small is beautiful. Cell 108, 13-16   DOI   ScienceOn
39 Aboshama, K. and Hansen, A. P. (1997) Effect of ultra-hightemperature steam sulfur-containing amino acids in milk. J. Dairy Sci. 60, 1374-78
40 Bruttin, A., Desiere, F., D'Amico, N., Guerin, J. P., Sidoti, J., Huni, B., Lucchini, S., and Brussow, H. (1997) Molecular ecology of Streptococcus thermophilus bacteriophage infections in a cheese factory. Appl. Environ. Microbiol. 63, 3144-3150   PUBMED
41 Coffey, A. G., Coakley, M., McGarry, A., Fitzgerald, G. F., and Ross, R. P. (1998) Increasing phage resistance of cheese starters: a case study using Lactococcus lactis DPC4268. Letters in Appl. Microbiol. 26, 51-55   DOI   ScienceOn
42 Sellars, R. L. (1981) Fermented dairy foods. J. Dairy Sci. 64, 1070-1076   DOI
43 Josephsen, J. and Neve, H. (2004) Lactic acid bacteria: microbiological and functional aspects. 3th ed. Marcel Dekker, Inc.
44 McGrath, S., Neve, H., Seegers, J. F. M. L., Eijlander, R., Vegge, C. S., Brondsted, L., Heller, K. J., Fitzgerald, G. F., Vogensen, F. K., and Sinderen, D. (2006) Anatomy of a lactococcal phage tail. J. Bacteriol. 188, 3972–3982   DOI   ScienceOn
45 Sanlibaba, P. and Akcelik, M. (2005) Classification of virulent lactococcal bacteriophages based on protein composition and restriction endonuclease analysis. Turk. J. Vet. Anim. Sci. 29, 865-871
46 Le Marrec, C., van Sinderen, D., Walsh, L., Stanley, E., Vlegels, E., Moineau, S., Heinze, P., Fitzgerald, G., and Fayard, B. (1997) Streptococcus thermophilus bacteriophages can be divided into two distinct groups based on mode of packaging and structural protein composition. Appl. Environ. Microbiol. 63, 3246-3253   PUBMED
47 McGrath, S., Fitzgerald, G. F., and Sinderen, D. V. (2004b) The impact of bacteriophage genomics. Curr. Opin. Biotechnol. 15, 94-99   DOI   ScienceOn
48 Moroni, O., Jean, J., Autret, J., and Fliss, I. (2002) Inactivation of lactococcal bacteriophages in liquid media using dynamic high pressure. Int. Dairy J. 12, 907-913   DOI   ScienceOn
49 Muller, M., Rauscher, M. T., and Hinrichs, J. (2005) Inactivation of bacteriophages by thermal and high-pressure treatment. Int. Dairy J. 15, 777-784   DOI   ScienceOn
50 Nelson, D., Schuch, R., Chahales, P., Zhu, S., and Fischetti, V. A. (2006) A multimeric bacteriophage lysin. Proc. Natl. Acad. Sci. USA 103, 10765-10770   DOI   ScienceOn
51 Whitehead, H. R. and Hunter, G. J. E. (1945) Bacteriophage infection in cheese manufacture. J. Dairy Res. 14, 64-80
52 Daly, C. (1983) Starter culture developments in Ireland. Ir. J. Food Sci. Technol. 7, 39-48
53 Norman, N. P. and Nelson, F. E. (1953) Role of calcium and related ions in proliferation of lactic Streptococcus bacteriophage. J. Bacteriol. 66, 508-516
54 Labrie, S. and Moineau, S. (2000) Multiple PCR for detection and identification of lactococcal bacteriophages. Appl. Environ. Microbiol. 66, 987-994   DOI   ScienceOn
55 Prevots, F., Mata, M., and Ritzenthaler, P. (1990) Taxonomic differentiation of 101 lactococcal bacteriophages with unusually large genomes. Appl. Environ. Microbiol. 56, 2180-2185   PUBMED
56 Wilkowske, H. H., Nelson, F. E., and Parmelee, C. E. (1954) Serological classification of bacteriophages active against lactic streptococci. Appl. Microbiol. 2, 243-249   PUBMED
57 Hill, C. (1993) Bacteriophage and bacteriophage resistance in lactic acid bacteria. FEMS Microbiol. Rev. 12, 87-108   DOI
58 Klaenhammer, T., Sanozky, R., and Steenson, L. (1990) pTR2030, a conjugal plasmid and derivatives thereof that confer phage reisistance to group N streptococci. Patents US 4931396, US 5139950
59 Neve, H., Krusch, U., and Teuber, M. (1989) Classification of virulent bacteriophages of Sreptococcus salivarius subsp thermophilus isolated from yogurt and swiss-type cheese. Appl. Microbiol. Biotechnol. 30, 624-629   DOI
60 Nichols, A. A. and Hoyle, M. (1949) Bacteriophage in typing lactic streptococci. J. Dairy Res. 16, 167-208   DOI
61 Zottola, E. A. and Marth. E. H. (1966) Thermal inactivation of bacteriophages active against lactic streptococci. J. Dairy Sci. 49, 1338-1342   DOI   ScienceOn
62 Avsaroglu, M. D. and Buzrul, S. (2007) Hypochlorite inactivation kinetics of lactococcal bacteriophages. Food Sci. Technol., 40, 1369-1375   DOI   ScienceOn
63 Fayard, B., Haeflinger, M., and Accolas, J. P. (1993) Interaction of temperate bacteriophahges of Strpeococcus salivarius subsp. thermophilus with lysogenic indicators affect phage DNA restriction patterns and host ranges. J. Dairy Sci. 60, 385-399
64 Jarvis, A. W. (1989) Bacteriophages of lactic acid bacteria. J. Dairy Sci. 72, 3406-3428   DOI
65 Shafia, F. and Thompson, T. L. (1964) Calcium ion requirement for proliferation of bacteriophage $\mu$-4. J. Bacteriol. 88, 293-296
66 Champiat, D., Creuly, C., and Larpent, J. P. (1988) Contr$\^{o}$le de l'activit$\ phagique par dosage de l'ATP chez les streptocoques lactiques mesophiles. Microbiol. Aliment. Nutr. 6, 285-288
67 Walstra, P., Geurts, T. J., Noomen, A., Jellema, A., and Van Boekel, M. (1999) Dairy technology: principles of milk properties and processes. Dekker. New York
68 Josephsen, J., Petersen, A., Neve, H., and Nielsen, E. W. (1999) Development of lytic Lactococcus lactis bacteriophages in a Cheddar cheese plant. Int. J. Food Microbiol. 50, 163-171   DOI   ScienceOn
69 Kivi, S., Peltomaki, T., Luomala, K., and Sarimo, S. S. (1987) Some properties of Streptococcus thermophoilus bacteriophages. Folia Microbiol. 32,101-106   DOI   PUBMED   ScienceOn
70 Moineau, S., Borkaev, M., Holler, B. J., Walker, S. A., Kondo, J. K., Vedamuthu, E. R., and Vanderbergh, P. A. (1993) Production of monoclonal antibodies against the major capsid protein of the lactococcus bacteriophage ul36 and development of an enzyme-linked immunosorbent assay for direct phage detection in whey and milk. Appl. Environ. Microbiol. 59, 2034-2040   PUBMED
71 Svenson, U. and Christansson, A. (1991) Methods for phage monitoring. Bull. Int. Dairy Fed. 263, 29-39
72 Binetti, A. G., Capra, M. L., Alvarez, M. A., and Reinheimer, J. A. (2008) PCR method for detection and identification of Lactobacillus casei / paracasei bacteriophages in dairy products. Int. J. Food. Microbiol. 124, 147-153   DOI   ScienceOn
73 Braun, V. Jr., Hertwig, S., Neve, H., Geis, A., and Teuber, M. (1989) Taxonomic differentiation of bacteriophages of Lactococcus lactis by electron microscopy, DNA-DNA hybridization, and protein profiles. J. Gen. Microbiol. 135, 2551-2560   DOI
74 Capra, M. L., Quiberoni, A., Ackermann, H. W., Moineau, S., and Reinheimer, J. A. (2006) Characterization of a new virulent phage (MLC-A) of Lactobacillus paracasei. J. Dairy Sci. 89, 2414-2423   DOI   ScienceOn
75 Forsman, P. and Alatossava, T. (1991) Genetic variation of Lactobacillus delbrueckii subsp. lactis bacteriophage isolated from cheese processing plants in Finland. Appl. Environ. Microbiol. 57, 1805-1812   PUBMED
76 Lawrence, R. C., Heap, H. A., and Limsowtin, G. (1978) Symposium: Research and development trends in natural cheese manufacturing and ripening. J. Dairy Sci. 61, 1181-1191   DOI
77 Daly, C. and Fitzgerald, G. (1991) Plasmids conferring phage insensitivity on bacteria. Patents EP 0246909, IE 66528, US 5019506
78 Heap, H. A. and Jarvi, A. W. (1980) A comparison of prolate and isometric headed lactic streptococcal bacteriophages. N. Z. J. Dairy Sci. Technol. 15, 75-81
79 Moineau, S., Borkaev, M., Holler, B. J., Walker, S. A., Kondo, J. K., Vedamuthu, E. R., and Vandenbergh, P. A. (1996) Isolation and characterization of lactococcal bacteriophages from cultured buttermilk plants in the United States. J. Dairy Sci. 79, 2104-2111   DOI   ScienceOn
80 Schereiber, R. and Hinrichs, J. (2000) Rennet coagulation of heated milk concentrates. Lait 80, 33-42   DOI   ScienceOn
81 Valles, E. (1955) Sur l'emploi de differents indicateurs d'oxydo-r$\duction pour l'$\tude des bact$\riophages des streptocoques lactiques. Lait 35, 241-258   DOI
82 Sozzi, P. T. (1972) Calcium requirements of lactic starter phages. Milchwissenschaft 27, 503-506
83 Svensson, U. K. (1994) Conductimetric analysis of bacteriophage infection of two groups of bacteria in DL-lactococcal starter culture. J. Dairy Sci. 77, 3524-3531   DOI   ScienceOn