Chapter 10 : Bacteriophages in Industrial Food Processing: Incidence and Control in Industrial Fermentation

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

Bacteriophages in Industrial Food Processing: Incidence and Control in Industrial Fermentation, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816629/9781555815028_Chap10-1.gif /docserver/preview/fulltext/10.1128/9781555816629/9781555815028_Chap10-2.gif


Fermentation has been used as a method of food preservation for millennia. Some modern food fermentations are still initiated using the indigenous bacterial micro-flora of the raw substrate, also referred to as spontaneous fermentation. From the nutrient-rich environments to extreme environments such as the human digestive tract or deep-ocean thermal vents, bacteriophages have been discovered. Bacteriophages are undoubtedly the greatest threat in fermented food productions, especially in the dairy industry, which has openly acknowledged this biotechnological problem. Starter cultures used by the dairy industry are composed of lactic acid bacteria, which represent a diverse group including, among others, the genera and as well as the species . The bacteriophages infecting these groups of bacteria have been extensively characterized because of their negative impact on the industry. For example, lactococcal phages are the most-studied group of bacterial viruses after the phages. Biochemical methods are based primarily on immunochemical assays and molecular detection of bacteriophage genetic material (most often double-stranded DNA). Biochemical detection techniques are essential in identifying an emerging phage population. Bacteriophage-insensitive mutants (BIMs) have the same genetic determinants and most likely the same desired metabolic properties as the wild-type strain. Bacterial restriction-modification (R-M) systems are recognized as among the first line of defense after foreign DNA entry into the cell. The emergence of resistant phages points to the necessity of continuing to identify new phage resistance mechanisms for long-term phage resistance in important bioindustries.

Citation: Labrie S, Moineau S. 2010. Bacteriophages in Industrial Food Processing: Incidence and Control in Industrial Fermentation, p 199-216. In Sabour P, Griffiths M (ed), Bacteriophages in the Control of Food-and Waterborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555816629.ch10

Key Concept Ranking

Cell Wall Proteins
Fermented Milk Products
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


1. Ackermann, H.-W. 2007. 5500 phages examined in the electron microscope. Arch. Virol. 152:227243.
2. Ackermann, H.-W. 2009. Basic phage electron microscopy, p. 113126. In M. R. J. Clokie and, A. M. Kropinski ,(ed.), Bacteriophages: Methods and Protocols, vol. 1. Isolation, Characterization, and Interactions. Humana Press, Springer, New York, NY.
3. Ackermann, H.-W.,, E. D. Cantor,, A. W. Jarvis,, J. Lembke, and, J. A. Mayo. 1984. New species definitions in phages of gram-positive cocci. Intervirology 22:181190.
4. Ackermann, H.-W.,, M. S. Dubow,, A. W. Jarvis,, L. A. Jones,, V. N. Krylov,, J. Maniloff,, J. Rocourt,, R. S. Safferman,, J. Schneider,, L. Seldin,, T. Sozzi,, P. R. Stewart,, M. Werquin, and, L. Wunsche. 1992. The species concept and its application to tailed phages. Arch. Virol. 124: 6982.
5. Akçelik, M. 1998. A phage DNA injection-blocking type resistance mechanism encoded by chromosomal DNA in Lactococcus lactis subsp. lactis PLM-18. Milchwissenschaft 53:619622.
6. Akçelik, M.,, P. Sanlibaba, and, Ç. Tükel. 2000. Phage resistance in Lactococcus lactis subsp. lactis strains isolated from traditional fermented milk products in Turkey. Int. J. Food Sci. Tech. 35:473481.
7. Allison, G. E., and, T. R. Klaenhammer. 1998. Phage resistance mechanisms in lactic acid bacteria. Int. Dairy J. 8:207226.
8. Babu, K. S.,, W. S. Spence,, M. R. Monteville, and, B. L. Geller. 1995. Characterization of a cloned gene (pip) from Lactococcus lactis required for phage infection. Dev. Biol. Stand. 85:569575.
9. Barrangou, R.,, C. Frémaux,, H. Deveau,, M. Richards,, P. Boyaval,, S. Moineau,, D. A. Romero, and, P. Horvath. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:17091712.
10. Binetti, A. G.,, B. Del Rio,, M. C. Martin, and, M. A. Alvarez. 2005. Detection and characterization of Streptococcus thermophilus bacteriophages by use of the antireceptor gene sequence. Appl. Environ. Microbiol. 71:60966103.
11. Bissonnette, F.,, S. Labrie,, H. Deveau,, M. Lamoureux, and, S. Moineau. 2000. Characterization of mesophilic mixed starter cultures used for the manufacture of aged cheddar cheese. J. Dairy Sci. 83:620627.
12. Bogosian, G. 2005. Control of bacteriophage in commercial microbiology and fermentation facilities, p. 667674. In R. Calendar (ed.), The Bacteriophages, 2nd ed. Oxford University Press, New York, NY.
13. Bolotin, A.,, B. Ouinquis,, A. Sorokin, and, S. D. Ehrlich. 2005. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151:25512561.
14. Bolotin, A.,, P. Wincker,, S. Mauger,, O. Jaillon,, K. Malarme,, J. Weissenbach,, S. D. Ehrlich, and, A. Sorokin. 2001. The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res. 11:731753.
15. Bossi, L.,, J. A. Fuentes,, G. Mora, and, N. Figueroa-Bossi. 2003. Prophage contribution to bacterial population dynamics. J. Bacteriol. 185:64676471.
16. Bouchard, J. D., and, S. Moineau. 2000. Homologous recombination between a lactococcal bacteriophage and the chromosome of its host strain. Virology 270:6575.
17. Boucher, I., and, S. Moineau. 2001. Phages of Lactococcus lactis: an ecological and economical equilibrium. Recent Res. Devel. Virol. 3:243256.
18. Braun, V., Jr.,, S. Hertwig,, H. Neve,, A. Geis, and, M. Teuber. 1989. Taxonomic differentiation of bacteriophages of Lactococcus lactis by electron microscopy, DNA-DNA hybridization, and protein profiles. J. Gen. Microbiol. 135:25512560.
19. Breitbart, M., and, F. Rohwer. 2005. Here a virus, there a virus, everywhere the same virus? Trends Microbiol. 13:278284.
20. Brenner, S., and, R. W. Horne. 1959. A negative staining method for high resolution electron microscopy of viruses. Biochim. Biophys. Acta 34:103110.
21. Brüssow, H.,, C. Canchaya, and, W. D. Hardt. 2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68:560602.
22. Brüssow, H., and, R. W. Hendrix. 2002. Phage genomics: small is beautiful. Cell 108:1316.
23. Canchaya, C.,, C. Proux,, G. Fournous,, A. Bruttin, and, H. Brüssow. 2003. Prophage genomics. Microbiol. Mol. Biol. Rev. 67:238276.
24. Capra, M. L.,, A. Quiberoni, and, J. A. Reinheimer. 2004. Thermal and chemical resistance of Lactobacillus casei and Lactobacillus paracasei bacteriophages. Lett. Appl. Microbiol. 38:499504.
25. Casjens, S. 2003. Prophages and bacterial genomics: what have we learned so far? Mol. Microbiol. 49:277300.
26. Chibani Azaiez, S. R.,, I. Fliss,, R. E. Simard, and, S. Moineau. 1998. Monoclonal antibodies raised against native major capsid proteins of lactococcal c2-like bacteriophages. Appl. Environ. Microbiol. 64:42554259.
27. Chopin, M.-C. 1980. Resistance of 17 mesophilic lactic Streptococcus bacteriophages to pasteurization and spray-drying. J. Dairy Res. 47:131139.
28. Chopin, M.-C.,, A. Chopin, and, E. Bidnenko. 2005. Phage abortive infection in lactococci: variations on a theme. Curr. Opin. Microbiol. 8:473479.
29. Coffey, A., and, R. P. Ross. 2002. Bacteriophage-resistance systems in dairy starter strains: molecular analysis to application. Antonie van Leeuwenhoek 82:303321.
30. Deveau, H.,, R. Barrangou,, J. E. Garneau,, J. Labonte,, C. Fremaux,, P. Boyaval,, D. A. Romero,, P. Horvath, and, S. Moineau. 2008. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol. 190:13901400.
31. Deveau, H.,, S. J. Labrie,, M.-C. Chopin, and, S. Moineau. 2006. Biodiversity and classification of lactococcal phages. Appl. Environ. Microbiol. 72:43384346.
32. Djordjevic, G., and, T. Klaenhammer. 1997. Bacteriophage-triggered defense systems: phage adaptation and design improvements. Appl. Environ. Microbiol. 63:43704376.
33. Djordjevic, G. M.,, D. J. O’Sullivan,, S. A. Walker,, M. A. Conkling, and, T. R. Klaenhammer. 1997. A triggered-suicide system designed as a defense against bacteriophages. J. Bacteriol. 179:67416748.
34. Dupont, K.,, F. K. Vogensen, and, J. Josephsen. 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. 98:10011009.
35. Durmaz, E., and, T. R. Klaenhammer. 2000. Genetic analysis of chromosomal regions of Lactococcus lactis acquired by recombinant lytic phages. Appl. Environ. Microbiol. 66:895903.
36. Émond, É., and, S. Moineau. 2007. Bacteriophages and food fermentation, p. 93124. In S. McGrath and, D. van Sinderen (ed.), Bacteriophage: Genetics and Molecular Biology. Caister Academic Press, Norfolk, United Kingdom.
37. Fineran, P. C.,, T. R. Blower,, I. J. Foulds,, D. P. Humphreys,, K. S. Lilley, and, G. P. C. Salmond. 2009. The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc. Natl. Acad. Sci. USA 106:894899.
38. Forde, A., and, G. F. Fitzgerald. 1999a. Analysis of exopolysaccharide (EPS) production mediated by the bacteriophage adsorption blocking plasmid, pCI658, isolated from Lactococcus lactis ssp. cremoris HO2. Int. Dairy J. 9:465472.
39. Forde, A., and, G. F. Fitzgerald. 1999b. Bacteriophage defence systems in lactic acid bacteria. Antonie van Leeuwenhoek 76:89113.
40. Garbutt, K. C.,, J. Kraus, and, B. L. Geller. 1997. Bacteriophage resistance in Lactococcus lactis engineered by replacement of a gene for a bacteriophage receptor. J. Dairy Sci. 80:15121519.
41. Garvey, P.,, C. Hill, and, G. Fitzgerald. 1996. The lactococcal plasmid pNP40 encodes a third bacteriophage resistance mechanism, one which affects phage DNA penetration. Appl. Environ. Microbiol. 62:676679.
42. Geller, B. L.,, R. G. Ivey,, J. E. Trempy, and, B. Hettinger-Smith. 1993. Cloning of a chromosomal gene required for phage infection of Lactococcus lactis subsp. lactis C2. J. Bacteriol. 175:55105519.
43. Giraffa, G. 2004. Studying the dynamics of microbial populations during food fermentation. FEMS Microbiol. Rev. 28:251260.
44. Godde, J. S., and, A. Bickerton. 2006. The repetitive DNA elements called CRISPRs and their associated genes: evidence of horizontal transfer among prokaryotes. J. Mol. Evol. 62:718729.
45. Gullo, M., and, P. Giudici. 2008. Acetic acid bacteria in traditional balsamic vinegar: phenotypic traits relevant for starter cultures selection. Int. J. Food Microbiol. 125:4653.
46. Haft, D. H.,, J. Selengut,, E. F. Mongodin, and, K. E. Nelson. 2005. A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comp. Biol. 1:474483.
47. Häring, M.,, X. Peng,, K. Brügger,, R. Rachel,, K. O. Stetter,, R. A. Garrett, and, D. Prangishvili. 2004. Morphology and genome organization of the virus PSV of the hyperthermophilic archaeal genera Pyrobaculum and Thermoproteus: a novel virus family, the Globuloviridae. Virology 323:233242.
48. Häring, M.,, R. Rachel,, X. Peng,, R. A. Garrett, and, D. Prangishvili. 2005a. Viral diversity in hot springs of Pozzuoli, Italy, and characterization of a unique archaeal virus, acidianus bottle-shaped virus, from a new family, the Ampullaviridae. J. Virol.79:99049911.
49. Häring, M.,, G. Vestergaard,, R. Rachel,, L. M. Chen,, R. A. Garrett, and, D. Prangishvili. 2005b. Independent virus development outside a host. Nature 436:11011102.
50. Horvath, P.,, D. A. Romero,, A.-C. Coute-Monvoisin,, M. Richards,, H. Deveau,, S. Moineau,, P. Boyaval,, C. Fremaux, and, R. Barrangou. 2008. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J. Bacteriol. 190:14011412.
51. Hutkins, R. W. 2006. Microbiology and Technology of Fermented Foods. Blackwell Publishing, Chicago, IL.
52. Jansen, R.,, J. D.A. van Embden,, W. Gaastra, and, L. M. Schouls. 2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43:15651575.
53. Jarvis, A. W. 1984. Differentiation of lactic streptococcal phages into phage species by DNA-DNA homology. Appl. Environ. Microbiol. 47:343349.
54. Jarvis, A. W.,, G. F. Fitzgerald,, M. Mata,, A. Mercenier,, H. Neve,, I. B. Powell,, C. Ronda,, M. Saxelin, and, M. Teuber. 1991. Species and type phages of lactococcal bacteriophages. Intervirology 32:29.
55. Kang, Y. J., and, J. F. Frank. 1989. Biological aerosols—a review of airborne contamination and its measurement in dairy processing plants. J. Food Prot. 52:512524.
56. Labrie, S., and, S. Moineau. 2000. Multiplex PCR for detection and identification of lactococcal bacteriophages. Appl. Environ. Microbiol. 66:987994.
57. Labrie, S. J., and, S. Moineau. 2007. Abortive infection mechanisms and prophage sequences significantly influence the genetic makeup of emerging lytic lactococcal phages. J. Bacteriol. 189:14821487.
58. Ledeboer, A. M.,, S. Bezemer,, J. J. de Haard,, I. M. Schäffers,, C. T. Verrips,, C. van Vliet,, E. M. Dusterhoft,, P. Zoon,, S. Moineau, and, L. G. Frenken. 2002. Preventing phage lysis of Lactococcus lactis in cheese production using a neutralizing heavy-chain antibody fragment from llama. J. Dairy Sci. 85:13761382.
59. Le Marrec, C.,, D. van Sinderen,, L. Walsh,, E. Stanley,, E. Vlegels,, S. Moineau,, P. Heinze,, G. Fitzgerald, and, B. Fayard. 1997. Two groups of bacteriophages infecting Streptococcus thermophilus can be distinguished on the basis of mode of packaging and genetic determinants for major structural proteins. Appl. Environ. Microbiol. 63:32463253.
60. Lembke, J., and, M. Teuber. 1981. Serotyping of morphologically identical bacteriophages of lactic streptococci by immunoelectronmicroscopy. Milchwissenschaft 36:1012.
61. Lévesque, C.,, M. Duplessis,, J. Labonté,, S. Labrie,, C. Fremaux,, D. Tremblay, and, S. Moineau. 2005. Genomic organization and molecular analysis of virulent bacteriophage 2972 infecting an exopolysaccharide-producing Streptococcus thermophilus strain. Appl. Environ. Microbiol. 71:40574068.
62. Lu, Z.,, F. Breidt,, H. P. Fleming,, E. Altermann, and, T. R. Klaenhammer. 2003. Isolation and characterization of a Lactobacillus plantarum bacteriophage, ϕJL-1, from a cucumber fermentation. Int. J. Food Microbiol. 84:225235.
63. Lucey, M.,, C. Daly, and, G. F. Fitzgerald. 1992. Cell-surface characteristics of Lactococcus lactis harboring pCI528, a 46 kb plasmid encoding inhibition of bacteriophage adsorption. J. Gen. Microbiol. 138:21372143.
64. Madera, C.,, C. Monjardin, and, J. E. Suarez. 2004. Milk contamination and resistance to processing conditions determine the fate of Lactococcus lactis bacteriophages in dairies. Appl. Environ. Microbiol. 70:73657371.
65. Makarova, K.,, A. Slesarev,, Y. Wolf,, A. Sorokin,, B. Mirkin,, E. Koonin,, A. Pavlov,, N. Pavlova,, V. Karamychev,, N. Polouchine,, V. Shakhova,, I. Grigoriev,, Y. Lou,, D. Rohksar,, S. Lucas,, K. Huang,, D. M. Goodstein,, T. Hawkins,, V. Plengvidhya,, D. Welker,, J. Hughes,, Y. Goh,, A. Benson,, K. Baldwin,, J. H. Lee,, I. Diaz-Muniz,, B. Dosti,, V. Smeianov,, W. Wechter,, R. Barabote,, G. Lorca,, E. Altermann,, R. Barrangou,, B. Ganesan,, Y. Xie,, H. Rawsthorne,, D. Tamir,, C. Parker,, F. Breidt,, J. Broadbent,, R. Hutkins,, D. O’Sullivan,, J. Steele,, G. Unlu,, M. Saier,, T. Klaenhammer,, P. Richardson,, S. Kozyavkin,, B. Weimer, and, D. Mills. 2006a. Comparative genomics of the lactic acid bacteria. Proc. Natl. Acad. Sci. USA 103:1561115616.
66. Makarova, K. S.,, N. V. Grishin,, S. A. Shabalina,, Y. I. Wolf, and, E. V. Koonin. 2006b. A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol. Direct 1:26.
67. Mazzocco, A.,, T. E. Waddell,, E. Lingohr, and, R. P. Johnson. 2009a. Enumeration of bacteriophages by the direct plating plaque assay, p. 7780. In M. R. J. Clokie and, A. M. Kropinski (ed.), Bacteriophages: Methods and Protocols, vol. 1. Isolation, Characterization, and Interactions. Humana Press, Springer, New York, NY.
68. Mazzocco, A.,, T. E. Waddell,, E. Lingohr, and, R. P. Johnson. 2009b. Enumeration of bacteriophages using the small drop plaque assay system, p. 8185. In M. R. J. Clokie and, A. M. Kropinski (ed.), Bacteriophages: Methods and Protocols, vol. 1. Isolation, Characterization, and Interactions. Humana Press, Springer, New York, NY.
69. McGrath, S.,, G. F. Fitzgerald, and, D. van Sinderen. 2002. Identification and characterization of phage-resistance genes in temperate lactococcal bacteriophages. Mol. Microbiol. 43:509520.
70. McGrath, S.,, G. F. Fitzgerald, and, D. van Sinderen. 2007. Bacteriophages in dairy products: pros and cons. Biotechnol. J. 2:450455.
71. McLoughlin, A. J., and, C. P. Champagne. 1994. Immobilized cells in meat fermentation. Crit. Rev. Biotechnol. 14:179192.
72. Moineau, S. 1999. Applications of phage resistance in lactic acid bacteria. Antonie van Leeuwenhoek 76:377382.
73. Moineau, S.,, D. Bernier,, M. Jobin,, J. Hebert,, T. Klaenhammer, and, S. Pandian. 1993. Production of monoclonal antibodies against the major capsid protein of the Lactococcus bacteriophage ul36 and development of an enzyme-linked immuno-sorbent assay for direct phage detection in whey and milk. Appl. Environ. Microbiol. 59:20342040.
74. Moineau, S.,, M. Borkaev,, B. J. Holler,, S. A. Walker,, J. K. Kondo,, E. R. Vedamuthu, and, P. A. Vandenbergh. 1996. Isolation and characterization of lactococcal bacteriophages form cultured buttermilk plants in the United States. J. Dairy Sci. 79:21042111.
75. Moineau, S.,, J. Fortier,, H.-W. Ackermann, and, S. Pandian. 1992. Characterization of lactococcal bacteriophages from Québec cheese plants. Can. J. Microbiol. 38:875882.
76. Moineau, S., and, C. Lévesque. 2005. Control of bacteriophages in industrial fermentations, p. 285296. In E. Kutter and, A. Sulakvelidze (ed.), Bacteriophages: Biology and Applications. CRC Press, Boca Raton, FL.
77. Mojica, F. J. M.,, C. Diez-Villasenor,, J. Garcia-Martinez, and, E. Soria. 2005. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60:174182.
78. Mudgal, P.,, F. Breidt,, S. R. Lubkin, and, K. P. Sandeep. 2006. Quantifying the significance of phage attack on starter cultures: a mechanistic model for population dynamics of phage and their hosts isolated from fermenting sauerkraut. Appl. Environ. Microbiol. 72:39083915.
79. Murata, A., and, K. Kitagawa. 1973. Mechanism of inactivation of bacteriophage JL by ascorbic acid. Agric. Biol. Chem. 37:11451151.
80. Murata, A.,, K. Kitagawa, and, R. Saruno. 1971. Inactivation of bacteriophages by ascorbic acid. Agric. Biol. Chem. 35:294296.
81. Murata, A.,, R. Oyadomari,, T. Ohashi, and, K. Kitagawa. 1975. Mechanism of inactivation of bacteriophage deltaA containing single-stranded-DNA by ascorbic acid. J. Nutr. Sci. Vitaminol. (Tokyo) 21:261269.
82. Murata, A., and, M. Uike. 1976. Mechanism of inactivation of bacteriophage MS2 containing single-stranded RNA by ascorbic acid. J. Nutr. Sci. Vitaminol. (Tokyo) 22:347354.
83. Nes, I. F., and, O. Sorheim. 1984. Effect of infection of a bacteriophage in a starter culture during the production of salami dry sausage—a model study. J. Food Sci. 49:337340.
84. Neve, H.,, A. Berger, and, K. J. Heller. 1995. A method for detecting and enumerating airborne virulent bacteriophage of dairy starter cultures. Kieler Milchw. Forsch. 47:193207.
85. Neve, H.,, A. Laborius, and, K. J. Heller. 2003. Testing of the applicability of battery-powered portable microbial air samplers for detection and enumeration of airborne Lactococcus lactis dairy bacteriophages. Kieler Milchw. Forsch. 55:301315.
86. Norrby, E. 2008. Nobel Prizes and the emerging virus concept. Arch. Virol. 153:11091123.
87. Ohnishi, M.,, K. Kurokawa, and, T. Hayashi. 2001. Diversification of Escherichia coli genomes: are bacteriophages the major contributors? Trends Microbiol. 9:481485.
88. Okafor, N. 2007. Modern Industrial Microbiology and Biotechnology. Science Publishers, Enfield, NH.
89. O’Sullivan, D. J.,, C. Hill, and, T. R. Klaenhammer. 1993. Effect of increasing the copy number of bacteriophage origins of replication, in trans, on incoming-phage proliferation. Appl. Environ. Microbiol. 59:24492456.
90. Pourcel, C.,, G. Salvignol, and, G. Vergnaud. 2005. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151:653663.
91. Prangishvili, D.,, R. A. Garrett, and, E. V. Koonin. 2006a. Evolutionary genomics of archaeal viruses: unique viral genomes in the third domain of life. Virus Res. 117:5267.
92. Prangishvili, D.,, G. Vestergaard,, M. Haring,, R. Aramayo,, T. Basta,, R. Rachel, and, R. A. Garrett. 2006b. Structural and genomic properties of the hyperthermophilic archaeal virus ATV with an extracellular stage of the reproductive cycle. J. Mol. Biol. 359:12031216.
93. Quiberoni, A.,, V. B. Suarez, and, J. A. Reinheimer. 1999. Inactivation of Lactobacillus helveticus bacteriophages by thermal and chemical treatments. J. Food Prot. 62:894898.
94. Rachel, R.,, M. Bettstetter,, B. P. Hedlund,, M. Haring,, A. Kessler,, K. O. Stetter, and, D. Prangishvili. 2002. Remarkable morphological diversity of viruses and virus-like particles in hot terrestrial environments. Arch. Virol. 147:24192429.
95. Sanders, M. E. 1999. Phages in industrial fermentations, p. 12441248. In A. Granoff and, R. G. Webster (ed.), Encyclopedia of Virology, 2nd ed. Academic Press, San Diego, CA.
96. Schmidt, R. H.,, M. M. Vargas,, K. L. Smith, and, J. J. Jezeski. 1985. The effect of ultra-high temperature milk processing on yogurt texture. J. Food Process. Preserv. 9:235240.
97. Schouler, C.,, C. Bouet,, P. Ritzenthaler,, X. Drouet, and, M. Mata. 1992. Characterization of Lactococcus lactis phage antigens. Appl. Environ. Microbiol. 58:24792484.
98. Sijtsma, L.,, N. Jansen,, W. C. Hazeleger,, J. T. M. Wouters, and, K. J. Hellingwerf. 1990. Cell-surface characteristics of bacteriophage-resistant Lactococcus lactis subsp. cremoris SK110 and its bacteriophage-sensitive variant SK112. Appl. Environ. Microbiol. 56:32303233.
99. Sing, W., and, T. Klaenhammer. 1993. A strategy for rotation of different bacteriophage defenses in a lactococcal single-strain starter culture system. Appl. Environ. Microbiol. 59:365372.
100. Stadhouders, J., and, G. J. M. Leenders. 1984. Spontaneously developed mixed-strain cheese starters: their behavior towards phages and their use in the Dutch cheese industry. Neth. Milk Dairy J. 38:157181.
101. Sturino, J. M., and, T. R. Klaenhammer. 2002. Expression of antisense RNA targeted against Streptococcus thermophilus bacteriophages. Appl. Environ. Microbiol. 68:588596.
102. Sturino, J. M., and, T. R. Klaenhammer. 2004a. Antisense RNA targeting of primase interferes with bacteriophage replication in Streptococcus thermophilus. Appl. Environ. Microbiol. 70:17351743.
103. Sturino, J. M., and, T. R. Klaenhammer. 2004b. Bacteriophage defense systems and strategies for lactic acid bacteria. Adv. Appl. Microbiol. 56:331378.
104. Sturino, J. M., and, T. R. Klaenhammer. 2006. Engineered bacteriophage-defence systems in bioprocessing. Nat. Rev. Microbiol. 4:395404.
105. Sturino, J. M., and, T. R. Klaenhammer. 2007. Inhibition of bacteriophage replication in Streptococcus thermophilus by subunit poisoning of primase. Microbiology 153:32953302.
106. Suarez, V. B., and, J. A. Reinheimer. 2002. Effectiveness of thermal treatments and biocides in the inactivation of Argentinian Lactococcus lactis phages. J. Food Prot. 65:17561759.
107. Sullivan, J. J. 1979. Air microbiology and dairy processing. Aust. J. Dairy Technol. 34:133138.
108. Trevors, K. E.,, R. A. Holley, and, A. G. Kempton. 1984. Effect of bacteriophage on the activity of lactic-acid starter cultures used in the production of fermented sausage. J. Food Sci. 49:650651.
109. Tuncer, Y., and, M. Akçelik. 2002. A protein which masks galactose receptor mediated phage susceptibility in Lactococcus lactis subsp. lactis MPL56. Int. J. Food Sci. Technol. 37:139144.
110. Vestergaard, G.,, S. A. Shah,, A. Bize,, W. Reitberger,, M. Reuter,, H. Phan,, A. Briegel,, R. Rachel,, R. A. Garrett, and, D. Prangishvili. 2008. Stygiolobus rod-shaped virus and the interplay of crenarchaeal rudiviruses with the CRISPR antiviral system. J. Bacteriol. 190:68376845.
111. Villion, M., and, S. Moineau. 2009. Bacteriophages of Lactobacillus. Front. Biosci. 14:16611683.
112. Wegmann, U.,, M. O’Connell-Motherway,, A. Zomer,, G. Buist,, C. Shearman,, C. Canchaya,, M. Ventura,, A. Goesmann,, M. J. Gasson,, O. P. Kuipers,, D. van Sinderen, and, J. Kok. 2007. Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp. cremoris MG1363. J. Bacteriol. 189:32563270.
113. Whithead, H. R., and, G. A. Cox. 1935. The occurence of bacteriophage in lactic streptococci. N. Z. J. Sci. Technol. 16:319.
114. Whitman, W. B.,, D. C. Coleman, and, W. J. Wiebe. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA 95:65786583.
115. Yoon, S. S.,, R. Barrangou-Poueys,, F. Breidt, and, H. P. Fleming. 2007. Detection and characterization of a lytic Pediococcus bacteriophage from the fermenting cucumber brine. J. Microbiol. Biotechnol. 17:262270.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error