Biodiversity of lactococcal bacteriophages isolated from 3 Gouda-type cheese-producing plants

Journal of Dairy Science

Volumn 96, Issue 8, 2013, Pages 4945-4957

  Murphy, James ^a   Royer, Bridget ^a   Mahony, Jennifer ^a   Hoyles, Lesley ^a   Heller, Knut ^b   Neve, Horst ^b   Bonestroo, Martin ^c   Nauta, Arjen ^c   van Sinderen, Douwe ^a,d  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b FEDERAL RESEARCH INSTITUTE OF NUTRITION AND FOOD   (Germany)

^c FRIESLANDCAMPINA   (Netherlands)

^d UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

936 type phage; Cheese whey; Lactic acid bacteria; Starter culture

Indexed keywords

936-TYPE PHAGE; ARTICLE; BACTERIOPHAGE; BIODIVERSITY; CHEESE; CHEESE WHEY; ELECTRON MICROSCOPY; FOOD HANDLING; ISOLATION AND PURIFICATION; LACTIC ACID BACTERIUM; LACTOCOCCUS; METABOLISM; MICROBIOLOGY; MULTIPLEX POLYMERASE CHAIN REACTION; STARTER CULTURE; VIROLOGY;

936-TYPE PHAGE; CHEESE WHEY; LACTIC ACID BACTERIA; STARTER CULTURE;

BACTERIOPHAGES; BIODIVERSITY; CHEESE; FOOD TECHNOLOGY; LACTOCOCCUS; MICROSCOPY, ELECTRON; MULTIPLEX POLYMERASE CHAIN REACTION;

BACTERIA (MICROORGANISMS); LACTOCOCCUS LACTIS;

EID: 84880622625     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2013-6748     Document Type: Article

References (50)

1. Atamer Z., Dietrich J., Müller-Merbach M., Neve H., Heller K.J., Hinrichs J. Screening for and characterization of Lactococcus lactis bacteriophages with high thermal resistance. Int. Dairy J. 2009, 19:228-235.
2. Atamer Z., Hinrichs J. Thermal inactivation of the heat-resistant Lactococcus lactis bacteriophage P680 in modern cheese processing. Int. Dairy J. 2009, 20:163-168.
3. Bebeacua C., Lai L., Vegge C.S., Brondsted L., van Heel M., Veesler D., Cambillau C. Visualizing a complete Siphoviridae member by single-particle electron microscopy: The structure of lactococcal phage TP901-1. J. Virol. 2013, 87:1061-1068.
4. Braun J.V., Hertwig S., Neve H., Geis A., Teuber M. Taxonomic differentiation of bacteriophages of Lactococcus lactis by electron microscopy, DNA-DNA hybridization, and protein profiles. J. Gen. Microbiol 1989, 135:2551-2560.
5. Capra M.L., Neve H., Sorati P.C., Atamer Z., Hinrichs J., Heller K.J., Quiberoni A. Extreme thermal resistance of phages isolated from dairy samples: Updating traditional phage detection methodologies. Int. Dairy J. 2013, 30:59-63.
6. Casey C.N., Morgan E., Daly C., Fitzgerald G.F. Characterization and classification of virulent lactococcal bacteriophages isolated from a Cheddar cheese plant. J. Appl. Microbiol. 1993, 74:268-275.
7. Castro-Nallar E., Chen H., Gladman S., Moore S.C., Seemann T., Powell I.B., Hillier A., Crandall K.A., Chandry P.S. Population genomics and phylogeography of an Australian dairy factory derived lytic bacteriophage. Genome Biol. Evol. 2012, 4:382-393.
8. Chapot-Chartier M.P., Vinogradov E., Sadovskaya I., Andre G., Mistou M.Y., Trieu-Cuot P., Furlan S., Bidnenko E., Courtin P., Pechoux C., Hols P., Dufrene Y.F., Kulakauskas S. Cell surface of Lactococcus lactis is covered by a protective polysaccharide pellicle. J. Biol. Chem. 2010, 285:10464-10471.
9. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987, 162:156-159.
10. Chopin A., Chopin M.C., Moillo-Batt A., Langella P. Two plasmid-determined restriction and modification systems in Streptococcus lactis. Plasmid 1984, 11:260-263.
11. Crutz-Le Coq A.M., Cantele F., Lanzavecchia S., Marco S. Insights into structural proteins of 936-type virulent lactococcal bacteriophages. Arch. Virol. 2006, 151:1039-1053.
12. Deveau H., Labrie S.J., Chopin M.C., Moineau S. Biodiversity and classification of lactococcal phages. Appl. Environ. Microbiol. 2006, 72:4338-4346.
13. Dupont K., Vogensen F.K., Josephsen J. 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. 2005, 98:1001-1009.
14. Dupont K., Vogensen F.K., Neve H., Bresciani J., Josephsen J. Identification of the receptor-binding protein in 936-species lactococcal bacteriophages. Appl. Environ. Microbiol. 2004, 70:5818-5824.
15. Eller M.R., Dias R.S., De Moraes C.A., De Carvalho A.F., Oliveira L.L., Silva E.A., da Silva C.C., De Paula S.O. Molecular characterization of a new lytic bacteriophage isolated from cheese whey. Arch. Virol. 2012, 157:2265-2272.
16. Emond E., Moineau S. Bacteriophages and food fermentations Bacteriophage: Genetics and Molecular Biology 2007, 93-124. Scientific Press/Caister Academic Press, Norfolk, UK.
17. Garvey P., v.Sinderen D., Twomey D.P., Hill C., Fitzgerald G.F. Molecular genetics of bacteriophages and natural phage defense systems in the genus Lactococcus. Int. Dairy J. 1995, 5:905-947.
18. Gasson M.J. Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J. Bacteriol. 1983, 154:1-9.
19. Guglielmotti D.M., Mercanti D.J., Reinheimer J.A., Quiberoni Adel L. Review: Efficiency of physical and chemical treatments on the inactivation of dairy bacteriophages. Front Microbiol 2011, 2:282.
20. Harrigan W.F. Laboratory Methods in Food Microbiology 1998, Academic Press/Gulf Professional Publishing, San Diego, CA. 3rd.
21. Hejnowicz M.S., Golebiewski M., Bardowski J. Analysis of the complete genome sequence of the lactococcal bacteriophage bIBB29. Int. J. Food Microbiol. 2009, 131:52-61.
22. Hussain K., Masud T., Maqsud S., Mahmood T. Characterization of Lactococcus phages from Dahi whey. Pak. J. Nutr. 2008, 75:689-694.
23. Josephsen J., Petersen P., Neve H., Nielsen E.W. Development of lytic Lactococcus lactis bacteriophages in a Cheddar cheese plant. Int. J. Food Microbiol. 1999, 50:163-171.
24. Kenny J.G., Leach S., de la Hoz A.B., Venema G., Kok J., Fitzgerald G.F., Nauta A., Alonso J.C., van Sinderen D. Characterization of the lytic-lysogenic switch of the lactococcal bacteriophage Tuc2009. Virology 2006, 347:434-446.
25. Kleppen H.P., Bang T., Nes I.F., Holo H. Bacteriophages in milk fermentations: Diversity fluctuations of normal and failed fermentations. Int. Dairy J. 2011, 21:592-600.
26. Labrie S., Moineau S. Multiplex PCR for detection and identification of lactococcal bacteriophages. Appl. Environ. Microbiol. 2000, 66:987-994.
27. Labrie S.J., Josephsen J., Neve H., Vogensen F.K., Moineau S. Morphology, genome sequence, and structural proteome of type phage P335 from Lactococcus lactis. Appl. Environ. Microbiol. 2008, 74:4636-4644.
28. Lillehaug D. An improved plaque assay for poor plaque-producing temperate lactococcal bacteriophages. J. Appl. Microbiol. 1997, 83:85-90.
29. Lubbers M.W., Waterfield N.R., Beresford T.P., Le Page R.W., Jarvis A.W. Sequencing and analysis of the prolate-headed lactococcal bacteriophage c2 genome and identification of the structural genes. Appl. Environ. Microbiol. 1995, 61:4348-4356.
30. Mahony J., Deveau H., Mc Grath S., Ventura M., Canchaya C., Moineau S., Fitzgerald G.F., van Sinderen D. Sequence and comparative genomic analysis of lactococcal bacteriophages jj50, 712 and P008: Evolutionary insights into the 936 phage species. FEMS Microbiol. Lett. 2006, 261:253-261.
31. Mahony J., Murphy J., van Sinderen D. Lactococcal 936-type phages and dairy fermentation problems: From detection to evolution and prevention. Front Microbiol 2012, 3:335.
32. Mc Grath S., Neve H., Seegers J.F., Eijlander R., Vegge C.S., Brondsted L., Heller K.J., Fitzgerald G.F., Vogensen F.K., van Sinderen D. Anatomy of a lactococcal phage tail. J. Bacteriol. 2006, 188:3972-3982.
33. Miklič A., Rogelj I. Characterization of lactococcal bacteriophages isolated from Slovenian dairies. Int. J. Food Sci. Technol. 2003, 38:305-311.
34. Mills S., Griffin C., O'Sullivan O., Coffey A., McAuliffe O.E., Meijer W.C., Serrano L.M., Ross P.R. A new phage on the Mozzarella block: Bacteriophage 5093 shares a low level of homology with other Streptococcus thermophilus phages. Int. Dairy J. 2011, 21:963-969.
35. Moineau S., Fortier J., Ackermann H.W., Pandian S. Characterization of lactococcal bacteriophages from Quebec cheese plants. Can. J. Microbiol. 1992, 38:875-882.
36. Müller-Merbach M., Neve H., Hinrichs J. Kinetics of the thermal inactivation of the Lactococcus lactis bacteriophage P008. J. Dairy Res. 2005, 72:281-286.
37. Obregón V., Garcia J.L., Garcia E., Lopez R., Garcia P. Genome organization and molecular analysis of the temperate bacteriophage MM1 of Streptococcus pneumoniae. J. Bacteriol. 2003, 185:2362-2368.
38. Pillidge C.J., Jarvis A.W. DNA restriction maps and classification of the lactococcal bacteriophages c2 and sk1. J. Dairy Sci. Technol. 1988, 23:411-416.
39. Quiberoni A., Guglielmotti D.M., Reinheimer J.A. Inactivation of Lactobacillus delbrueckii bacteriophages by heat and biocides. Int. J. Food Microbiol. 2003, 84:51-62.
40. Raiski A., Belyasova N. Biodiversity of Lactococcus lactis bacteriophages in the Republic of Belarus. Int. J. Food Microbiol. 2009, 130:1-5.
41. Reddy P.S., Nair S., Mallikarjuna G., Kaul T., Markandeya G., Sopory S.K., Reddy M.K. A high-throughput, low-cost method for the preparation of "sequencing-ready" phage DNA template. Anal. Biochem. 2008, 376:258-261.
42. Rousseau G.M., Moineau S. Evolution of Lactococcus lactis phages within a cheese factory. Appl. Environ. Microbiol. 2009, 75:5336-5344.
43. Shepherd D.A., Veesler D., Lichiere J., Ashcroft A.E., Cambillau C. Unraveling lactococcal phage baseplate assembly by mass spectrometry. Mol. Cell. Proteomics 2011, 10. M111009787.
44. Sing W.D., Klaenhammer T.R. A strategy for rotation of different bacteriophage defenses in a lactococcal single-strain starter culture system. Appl. Environ. Microbiol. 1993, 59:365-372.
45. Szczepańska A.K., Hejnowicz M.S., Kolakowski P., Bardowski J. Biodiversity of Lactococcus lactis bacteriophages in Polish dairy environment. Acta Biochim. Pol. 2007, 54:151-158.
46. Tremblay D.M., Tegoni M., Spinelli S., Campanacci V., Blangy S., Huyghe C., Desmyter A., Labrie S., Moineau S., Cambillau C. Receptor-binding protein of Lactococcus lactis phages: Identification and characterization of the saccharide receptor-binding site. J. Bacteriol. 2006, 188:2400-2410.
47. Vegge C.S., Vogensen F.K., Mc Grath S., Neve H., van Sinderen D., Brondsted L. Identification of the lower baseplate protein as the antireceptor of the temperate lactococcal bacteriophages TP901-1 and Tuc2009. J. Bacteriol. 2006, 188:55-63.
48. Verreault D., Gendron L., Rousseau G.M., Veillette M., Masse D., Lindsley W.G., Moineau S., Duchaine C. Detection of airborne lactococcal bacteriophages in cheese manufacturing plants. Appl. Environ. Microbiol. 2011, 77:491-497.
49. Wegmann U., O'Connell-Motherway M., Zomer A., Buist G., Shearman C., Canchaya C., Ventura M., Goesmann A., Gasson M.J., Kuipers O.P., van Sinderen D., Kok J. Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis ssp. cremoris MG1363. J. Bacteriol. 2007, 189:3256-3270.
50. Whitehead H.R., Cox G.A. The occurrence of bacteriophage in cultures of lactic streptococci. N.Z. J. Sci. Technol. 1935, 16:319-320.