Phages of non-dairy lactococci: Isolation and characterization of φl47, a phage infecting the grass isolate lactococcus lactis ssp. Cremoris dpc6860

Frontiers in Microbiology

Volumn 4, Issue JAN, 2013, Pages

  Cavanagh, Daniel ^a,b   Guinane, Caitriona M ^a   Neve, Horst ^c   Coffey, Aidan ^d   Ross, R Paul ^a   Fitzgerald, Gerald F ^b   McAuliffe, Olivia ^a  

^a TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

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

^d Ireland   (Ireland)

Author keywords

Genome; Lactococcus lactis; Non dairy; Phage; Tail fiber

Indexed keywords

BACTERIOPHAGE DNA; DOUBLE STRANDED DNA; STRUCTURAL PROTEIN; TRANSFER RNA; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIOPHAGE; BACTERIOPHAGE L 47; BACTERIOPHAGE PHI 949; CYTOLYSIS; DNA REPLICATION; DNA SEQUENCE; ENZYME LINKED IMMUNOSPOT ASSAY; GENE CLUSTER; GENOME ANALYSIS; GENOME SIZE; HOST RANGE; LACTOCOCCUS LACTIS CREMORIS; NONHUMAN; NUCLEOTIDE METABOLISM; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PROTEIN ANALYSIS; RNA GENE; SEQUENCE HOMOLOGY; SEWAGE; TRANSMISSION ELECTRON MICROSCOPY; VIRION; VIRUS ATTACHMENT; VIRUS CAPSID; VIRUS CHARACTERIZATION; VIRUS GENE; VIRUS GENOME; VIRUS ISOLATION; VIRUS MORPHOLOGY; VIRUS TAIL;

EID: 84893647811     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00417     Document Type: Article

References (79)

1. Alander, M., Satokari, R., Korpela, R., Saxelin, M., Vilpponen-Salmela, T., Mattila-Sandholm, T., et al. (1999). Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption. Appl. Environ. Microbiol. 65, 351-354.
2. Alemayehu, D., Ross, R. P., O'Sullivan, O., Coffey, A., Stanton, C., Fitzgerald, G. F., et al. (2009). Genome of a virulent bacteriophage Lb338-1 that lyses the probiotic Lactobacillus paracasei cheese strain. Gene 448, 29-39. doi: 10.1016/j.gene.2009.08.008
3. Altermann, E., and Klaenhammer, T. R. (2003). GAMOLA: a new local solution for sequence annotation and analyzing draft and finished prokaryotic genomes. OMICS 7, 161-169. doi: 10.1089/153623103322246557
4. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410. doi: 10.1016/S0022-2836(05)80360-2
5. Ayad, E. H. E., Verheul, A., De Jong, C., Wouters, J. T. M., and Smit, G. (1999). Flavour forming abilities and amino acid requirements of Lactococcus lactis strains isolated from artisanal and non-dairy origin. Int. Dairy J. 9, 725-735. doi: 10.1016/s0958-6946(99)00140-5
6. Ayad, E. H. E., Verheul, A., Wouters, J. T. M., and Smit, G. (2000). Application of wild starter cultures for flavour development in pilot plant cheese making. Int. Dairy J. 10, 169-179. doi: 10.1016/s0958-6946(00)00041-8
7. Aziz, R. K., Bartels, D., Best, A. A., Dejongh, M., Disz, T., Edwards, R. A., et al. (2008). The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. doi: 10.1186/1471-2164-9-75
8. Bailly-Bechet, M., Vergassola, M., and Rocha, E. (2007). Causes for the intriguing presence of tRNAs in phages. Genome Res. 17, 1486-1495. doi: 10.1101/gr.6649807
9. Boulanger, P., Jacquot, P., Plançon, L., Chami, M., Engel, A., Parquet, C., et al. (2008). Phage T5 straight tail fiber is a multifunctional protein acting as a tape measure and carrying fusogenic and muralytic activities. J. Biol. Chem. 283, 13556-13564. doi: 10.1074/jbc.M800052200
10. Brüssow, H., and Desiere, F. (2001). Comparative phage genomics and the evolution of Siphoviridae: insights from dairy phages. Mol. Microbiol. 39, 213-223. doi: 10.1046/j.1365-2958.2001.02228.x
11. Brussow, H., and Kutter, E. (2005). "Genomics and evolution of tailed phages," in Bacteriophages: Biology and Applications, eds E. Kutter and A. Sulakvelidze (Washington, DC: CRC Press), 91-128.
12. Canchaya, C., Fournous, G., Chibani-Chennoufi, S., Dillmann, M.-L., and Brüssow, H. (2003). Phage as agents of lateral gene transfer. Curr. Opin. Microbiol. 6, 417-424. doi: 10.1016/S1369-5274(03)00086-9
13. Carver, T. J., Rutherford, K. M., Berriman, M., Rajandream, M. A., Barrell, B. G., and Parkhill, J. (2005). ACT: the Artemis Comparison Tool. Bioinformatics 21, 3422-3423. doi: 10.1093/bioinformatics/bti553
14. Ceska, T. A., and Sayers, J. R. (1998). Structure-specific DNA cleavage by 5′ nucleases. Trends Biochem. Sci. 23, 331-336. doi: 10.1016/S0968-0004(98)01259-6
15. Ceyssens, P.-J., Glonti, T., Kropinski, A. M., Lavigne, R., Chanishvili, N., Kulakov, L., et al. (2011). Phenotypic and genotypic variations within a single bacteriophage species. Virol. J. 8, 1-5. doi: 10.1186/1743-422X-8-134
16. Chevalier, B. S., and Stoddard, B. L. (2001). Homing endonucleases: structural and functional insight into the catalysts of intron/intein mobility. Nucleic Acids Res. 29, 3757-3774. doi: 10.1093/nar/29.18.3757
17. Chibani-Chennoufi, S., Bruttin, A., Dillmann, M.-L., and Brüssow, H. (2004a). Phage-host interaction: an ecological perspective. J. Bacteriol. 186, 3677-3686. doi: 10.1128/JB.186.12.3677-3686.2004
18. Chibani-Chennoufi, S., Dillmann, M.-L., Marvin-Guy, L., Rami-Shojaei, S., and Brüssow, H. (2004b). Lactobacillus plantarum bacteriophage LP65: a new member of the SPO1-like genus of the family Myoviridae. J. Bacteriol. 186, 7069-7083. doi: 10.1128/JB.186.21.7069-7083.2004
19. Chopin, A., Bolotin, A., Sorokin, A., Ehrlich, S. D., and Chopin, M. C. (2001). Analysis of six prophages in Lactococcus lactis IL1403: different genetic structure of temperate and virulent phage populations. Nucleic Acids Res. 29, 644-651. doi: 10.1093/nar/29.3.644
20. Chopin, A., Deveau, H., Ehrlich, S. D., Moineau, S., and Chopin, M.-C. (2007). KSY1, a lactococcal phage with a T7-like transcription. Virology 365, 1-9. doi: 10.1016/j.virol.2007.03.044
21. Coffey, A., and Ross, R. P. (2002). Bacteriophage-resistance systems in dairy starter strains: molecular analysis to application. Antonie van Leeuwenhoek 82, 303-321. doi: 10.1023/A:1020639717181
22. Crutz-Le Coq, A.-M., Cesselin, B., Commissaire, J., and Anba, J. (2002). Sequence analysis of the lactococcal bacteriophage bIL170: insights into structural proteins and HNH endonucleases in dairy phages. Microbiology 148, 985-1001.
23. Daniel, A., Bonnen, P. E., and Fischetti, V. A. (2007). First complete genome sequence of two Staphylococcus epidermidis bacteriophages. J. Bacteriol. 189, 2086-2100. doi: 10.1128/JB.01637-06
24. Delcher, A. L., Harmon, D., Kasif, S., White, O., and Salzberg, S. L. (1999). Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 27, 4636-4641. doi: 10.1093/nar/27.23.4636
25. Derbyshire, V., and Belfort, M. (1998). Lightning strikes twice: intron-intein coincidence. Proc. Natl. Acad. Sci. U.S.A. 95, 1356-1357. doi: 10.1073/pnas.95.4.1356
26. Desplats, C., and Krisch, H. M. (2003). The diversity and evolution of the T4-type bacteriophages. Res. Microbiol. 154, 259-267. doi: 10.1016/S0923-2508(03)00069-X
27. Deveau, H., Labrie, S. J., Chopin, M.-C., and Moineau, S. (2006). Biodiversity and classification of lactococcal phages. Appl. Environ. Microbiol. 72, 4338-4346. doi: 10.1128/AEM.02517-05
28. Dupuis, M.-È., and Moineau, S. (2010). Genome organization and characterization of the virulent lactococcal phage 1358 and its similarities to listeria phages. Appl. Environ. Microbiol. 76, 1623-1632. doi: 10.1128/aem.02173-09
29. Dwivedi, B., Xue, B., Lundin, D., Edwards, R. A., and Breitbart, M. (2013). A bioinformatic analysis of ribonucleotide reductase genes in phage genomes and metagenomes. BMC Evol. Biol. 13:1. doi: 10.1186/1471-2148-13-33
30. Ewing, B., and Green, P. (1998). Base-calling of automated sequencer traces usingPhred. II. error probabilities. Genome Res. 8, 186-194. doi: 10.1101/gr.8.3.175
31. Ferguson, P., and Coombs, D. (2000). Pulse-chase analysis of the in vivo assembly of the bacteriophage T4 tail. J. Mol. Biol. 297, 99-117. doi: 10.1006/jmbi.2000.3551
32. Fortier, L.-C., Bransi, A., and Moineau, S. (2006). Genome sequence and global gene expression of Q54, a new phage species linking the 936 and c2 phage species of Lactococcus lactis. J. Bacteriol. 188, 6101-6114. doi: 10.1128/JB.00581-06
33. Garneau, J. E., Tremblay, D. M., and Moineau, S. (2008). Characterization of 1706, a virulent phage from Lactococcus lactis with similarities to prophages from other Firmicutes. Virology 373, 298-309. doi: 10.1016/j.virol.2007.12.002
34. Gasteiger, E., Hoogland, C., Gattiker, A., Wilkins, M. R., Appel, R. D., and Bairoch, A. (2005). "Protein identification and analysis tools on the ExPASy server," in The Proteomics Protocols Handbook, ed J. M. Walker (New Jersey, NJ: Springer), 571-607.
35. Goodrich-Blair, H., and Shub, D. A. (1996). Beyond homing: competition between intron endonucleases confers a selective advantage on flanking genetic markers. Cell. 84, 211-221. doi: 10.1016/S0092-8674(00)80976-9
36. Gordon, D. (2003). Viewing and editing assembled sequences using Consed. Curr. Protoc. Bioinform. 2, 11.12.11-11.12.43. doi: 10.1002/0471250953.bi1102s02
37. Hatfull, G. F. (2002). A tail of two specifi-cities. Science. 295, 2031-2032. doi: 10.1126/science.1070586
38. Hawkins, S. A., Layton, A. C., Ripp, S., Williams, D., and Sayler, G. S. (2008). Genome sequence of the Bacteroides fragilis phage ATCC 51477-B1. Virol. J. 5, 97. doi: 10.1186/1743-422X-5-97
39. Hyatt, D., Chen, G.-L., Locascio, P., Land, M., Larimer, F., and Hauser, L. (2010). Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 11:1. doi: 10.1186/1471-2105-11-119
40. Jakutytë, L., Lurz, R., Baptista, C., Carballido-Lopez, R., São-José, C., Tavares, P., et al. (2012). First steps of bacteriophage SPP1 entry into Bacillus subtilis. Virology 422, 425-434. doi: 10.1074/jbc.M301805200
41. Jarvis, A. W. (1984). Differentiation of lactic streptococcal phages into phage species by DNA-DNA homology. Appl. Environ. Microbiol. 47, 343-349.
42. Jarvis, A. W., Fitzgerald, G. F., Mata, M., Mercenier, A., Neve, H., Powell, I. B., et al. (1991). Species and type phages of lactococcal bacteriophages. Intervirology 32, 2-9.
43. Juhala, R. J., Ford, M. E., Duda, R. L., Youlton, A., Hatfull, G. F., and Hendrix, R. W. (2000). Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J. Mol. Biol. 299, 27-51. doi: 10.1006/jmbi.2000.3729
44. Kato, H., Shiwa, Y., Oshima, K., Machii, M., Araya-Kojima, T., Zendo, T., et al. (2012). Complete genome sequence of Lactococcus lactis IO-1, a lactic acid bacterium that utilizes xylose and produces high levels of L-Lactic acid. J. Bacteriol. 194, 2102-2103. doi: 10.1128/JB.00074-12
45. Kelly, D., O'Sullivan, O., Mills, S., McAuliffe, O., Ross, P., Neve, H., et al. (2012). Genome sequence of the phage clP1, which infects the beer spoilage bacterium Pediococcus damnosus. Gene 504, 53-63. doi: 10.1016/j.gene.2012.04.085
46. Kelly, W. J., Ward, L. J. H., and Leahy, S. C. (2010). Chromosomal diversity in Lactococcus lactis and the origin of dairy starter cultures. Genome Biol. Evol. 2, 729-744. doi: 10.1093/gbe/evq056
47. Labrie, S. J., and Moineau, S. (2007). Abortive infection mechanisms and prophage sequences significantly influence the genetic makeup of emerging lytic lactococcal phages. J. Bacteriol. 189, 1482-1487. doi: 10.1128/JB.01111-06
48. Landthaler, M., Begley, U., Lau, N. C., and Shub, D. A. (2002). Two self-splicing group I introns in the ribonucleotide reductase large subunit gene of Staphylococcus aureus phage Twort. Nucleic Acids Res. 30, 1935-1943. doi: 10.1093/nar/30.9.1935
49. Laslett, D., and Canback, B. (2004). ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res. 32, 11-16. doi: 10.1093/nar/gkh152
50. Lowe, T. M., and Eddy, S. R. (1997). tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 0955-0964.
51. Lubbers, M. W., Waterfield, N. R., Beresford, T., Le Page, R., and Jarvis, A. W. (1995). Sequencing and analysis of the prolate-headed lactococcal bacteriophage c2 genome and identification of the structural genes. Appl. Environ. Microbiol. 61, 4348-4356.
52. Mahony, J., Martel, B., Tremblay, D. M., Neve, H., Heller, K. J., Moineau, S., et al. (2013). Identification of a new P335 subgroup through molecular analysis of lactococcal phages Q33 and BM13. Appl. Environ. Microbiol. 79, 4401-4409. doi: 10.1128/AEM.00832-13
53. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., Deweese-Scott, C., et al. (2011). CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39, D225-D229. doi: 10.1093/nar/gkq1189
54. 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: 10.1139/m92-143
55. Morales, P., Fernández-Garci{dotless}mathìA, E., Gaya, P., and Nuñez, M. (2003). Formation of volatile compounds by wild Lactococcus lactis strains isolated from raw ewes' milk cheese. Int. Dairy J. 13, 201-209. doi: 10.1016/s0958-6946(02)00151-6
56. Murphy, J., Royer, B., Mahony, J., Hoyles, L., Heller, K., Neve, H., et al. (2013). Biodiversity of lactococcal bacteriophages isolated from 3 Gouda-type cheese producing plants. J. Dairy Sci. 96, 4945-4957. doi: 10.3168/jds.2013-6748
57. Nowell, V. J., Kropinski, A. M., Songer, J. G., Macinnes, J. I., Parreira, V. R., and Prescott, J. F. (2012). Genome sequencing and analysis of a Type A Clostridium perfringens isolate from a case of bovine clostridial abomasitis. PLoS ONE 7:e32271. doi: 10.1371/journal.pone.0032271
58. O'Flaherty, S., Coffey, A., Edwards, R., Meaney, W., Fitzgerald, G. F., and Ross, R. P. (2004). Genome of staphylococcal phage K: a new lineage of Myoviridae infecting gram-positive bacteria with a low G+C content. J. Bacteriol. 186, 2862-2871. doi: 10.1128/JB.186.9.2862-2871.2004
59. Prevots, F., Mata, M., and Ritzenthaler, P. (1990). Taxonomic differentiation of 101 lactococcal bacteriophages and characterization of bacteriophages with unusually large genomes. Appl. Environ. Microbiol. 56, 2180-2185.
60. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M. A., et al. (2000). Artemis: sequence visualization and annotation. Bioinformatics 16, 944-945. doi: 10.1093/bioinformatics/16.10.944
61. Sambrook, J., and Russell, D. W. (2001). Molecular Cloning: a Laboratory Manual. Vol. 1-3. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
62. Samson, J. E., Magadán, A. H., Sabri, M., and Moineau, S. (2013). Revenge of the phages: defeating bacterial defences. Nat. Rev. Microbiol. 11, 675-687. doi: 10.1038/nrmicro3096
63. Samson, J. E., and Moineau, S. (2010). Characterization of Lactococcus lactis phage 949 and comparison with other lactococcal phages. Appl. Environ. Microbiol. 76, 6843-6852. doi: 10.1128/aem.00796-10
64. Sandmeier, H., Iida, S., and Arber, W. (1992). DNA inversion regions Min of plasmid p15B and Cin of bacteriophage P1: evolution of bacteriophage tail fiber genes. J. Bacteriol. 174, 3936-3944.
65. Schatz, M. C., Phillippy, A. M., Sommer, D. D., Delcher, A. L., Puiu, D., Narzisi, G., et al. (2013). Hawkeye and AMOS: visualizing and assessing the quality of genome assemblies. Brief. Bioinform. 14, 213-224. doi: 10.1093/bib/bbr074
66. Schuch, R., and Fischetti, V. A. (2006). Detailed genomic analysis of the Wβ and γ phages infecting Bacillus anthracis: implications for evolution of environmental fitness and antibiotic resistance. J. Bacteriol. 188, 3037-3051. doi: 10.1128/JB.188.8.3037-3051.2006
67. Seegers, J. F., Mc Grath, S., O'Connell-Motherway, M., Arendt, E. K., Van De Guchte, M., Creaven, M., et al. (2004). Molecular and transcriptional analysis of the temperate lactococcal bacteriophage Tuc2009. Virology. 329, 40-52. doi: 10.1016/j.virol.2004.07.003
68. Silhavy, T. J., Kahne, D., and Walker, S. (2010). The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2, 1-16. doi: 10.1101/cshperspect.a000414
69. Sjöberg, B. M., Hahne, S., Mathews, C. Z., Mathews, C. K., Rand, K. N., and Gait, M. J. (1986). The bacteriophage T4 gene for the small subunit of ribonucleotide reductase contains an intron. EMBO J. 5, 2031-2036.
70. Stockdale, S. R., Mahony, J., Courtin, P., Chapot-Chartier, M.-P., Van Pijkeren, J.-P., Britton, R. A., et al. (2013). The lactococcal phages Tuc2009 and TP901-1 incorporate two alternate forms of their tail fiber into their virions for infection specialization. J. Biol. Chem. 288, 5581-5590. doi: 10.1074/jbc.M112.444901
71. Sturino, J. M., and Klaenhammer, T. R. (2006). Engineered bacteriophage-defence systems in bioprocessing. Nat. Rev. Microbiol. 4, 395-404. doi: 10.1038/nrmicro1393
72. Suyama, M., and Bork, P. (2001). Evolution of prokaryotic gene order: genome rearrangements in closely related species. Trends Genet. 17, 10-13. doi: 10.1016/S0168-9525(00)02159-4
73. Uchiyama, J., Takemura, I., Satoh, M., Kato, S.-I., Ujihara, T., Akechi, K., et al. and Daibata, M. (2011). Improved adsorption of an enterococcus faecalis bacteriophage Φ EF24C with a spontaneous point mutation. PLoS ONE 6: e26648. doi: 10.1371/journal.pone.0026648
74. Urbach, G. (1995). Contribution of lactic acid bacteria to flavour compound formation in dairy products. Int. Dairy J. 5, 877-903. doi: 10.1016/0958-6946(95)00037-2
75. Veesler, D., and Cambillau, C. (2011). A common evolutionary origin for tailed-bacteriophage functional modules and bacterial machineries. Microbiol. Mol. Biol. Rev. 75, 423-433. doi: 10.1128/MMBR.00014-11
76. Vegge, C. S., Brøndsted, L., Neve, H., Mc Grath, S., Van Sinderen, D., and Vogensen, F. K. (2005). Structural characterization and assembly of the distal tail structure of the temperate lactococcal bacteriophage TP901-1. J. Bacteriol. 187, 4187-4197. doi: 10.1128/JB.187.12.4187-4197.2005
77. Villion, M., Chopin, M. C., Deveau, H., Ehrlich, S. D., Moineau, S., and Chopin, A. (2009). P087, a lactococcal phage with a morphogenesis module similar to an Enterococcus faecalis prophage. Virology 388, 49-56. doi: 10.1016/j.virol.2009.03.011
78. Weinbauer, M. G. (2004). Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28, 127-181. doi: 10.1016/j.femsre.2003.08.001
79. Young, P., Öhman, M., Xu, M. Q., Shub, D. A., and Sjöberg, B. M. (1994). Intron-containing T4 bacteriophage gene sunY encodes an anaerobic ribonucleotide reductase. J. Biol. Chem. 269, 20229-20232.