Involvement of the major capsid protein and two early-expressed phage genes in the activity of the lactococcal abortive infection mechanism AbiT

Applied and Environmental Microbiology

Volumn 78, Issue 19, 2012, Pages 6890-6899

  Labrie, Simon J ^a,b,d   Tremblay, Denise M ^a   Moisan, Maxim ^a,b   Villion, Manuela ^a,b   Magadán, Alfonso H ^a,b   Campanacci, Valérie ^c   Cambillau, Christian ^c   Moineau, Sylvain ^a,b  

^a UNIVERSITÉ LAVAL   (Canada)

^b Centre de Recherche sur les Matériaux Avancés CERMA   (Canada)

^c Centre National de la Recherche Scientifique   (France)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRAL ACTIVITIES; BIOINFORMATIC ANALYSIS; CAPSID PROTEINS; CO-EXPRESSION; COMPARATIVE GENOMIC; DAIRY INDUSTRY; FERMENTATION PROCESS; GENOMIC REGIONS; IMMUNOELECTRON MICROSCOPY; LACTIC ACID BACTERIA; LACTOCOCCUS LACTIS; MESOPHILIC; MODE OF ACTION; PHAGE CONTROL; PUTATIVE FUNCTIONS; WILD TYPES;

BACTERIOPHAGES; BIOINFORMATICS; DAIRY PRODUCTS; FERMENTATION; LACTIC ACID; PLANTS (BOTANY); RECOMBINANT PROTEINS;

GENES;

CAPSID PROTEIN;

ANTIMICROBIAL ACTIVITY; FERMENTATION; GENE EXPRESSION; GENOMICS; INFECTIVITY; MORPHOGENESIS; MUTATION; ORGANIC ACID; PROTEIN;

ARTICLE; BACTERIOPHAGE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOELECTRON MICROSCOPY; LACTOCOCCUS LACTIS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; ULTRASTRUCTURE; VIRION; VIROLOGY; VIRUS REPLICATION;

BACTERIOPHAGES; CAPSID PROTEINS; DNA MUTATIONAL ANALYSIS; GENE EXPRESSION REGULATION, VIRAL; LACTOCOCCUS LACTIS; MICROSCOPY, IMMUNOELECTRON; VIRION; VIRUS REPLICATION;

BACTERIA (MICROORGANISMS); LACTOCOCCUS LACTIS; MIRIDAE; POSIBACTERIA;

EID: 84868313344     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01755-12     Document Type: Article

References (65)

1. Altschul SF, et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Bennett-Lovsey RM, Herbert AD, Sternberg MJ, Kelley LA. 2008. Exploring the extremes of sequence/structure space with ensemble fold recognition in the program PHYRE. Proteins 70:611-625.
3. Bingham R, Ekunwe SIN, Falk S, Snyder L, Kleanthous C. 2000. The major head protein of bacteriophage T4 binds specifically to elongation factor Tu. J. Biol. Chem. 275:23219-23226.
4. Bissonnette F, Labrie S, Deveau H, Lamoureux M, Moineau S. 2000. Characterization of mesophilic mixed starter cultures used for the manufacture of aged cheddar cheese. J. Dairy Sci. 83:620-627.
5. Bouchard JD, Dion É, Bissonnette F, Moineau S. 2002. Characterization of the two-component abortive phage infection mechanism AbiT from Lactococcus lactis. J. Bacteriol. 184:6325-6332.
6. Bouchard JD, Moineau S. 2004. Lactococcal phage genes involved in sensitivity to AbiK and their relation to single-strand annealing proteins. J. Bacteriol. 186:3649-3652.
7. Casjens S, Hendrix R. 1988. Control mechanisms in dsDNA bacteriophage assembly, p 15-41. In Calendar R (ed), The bacteriophages. Plenum Press, New York, NY.
8. Chandry PS, Davidson BE, Hillier AJ. 1994. Temporal transcription map of the Lactococcus lactis bacteriophage sk1. Microbiology 140:2251-2261.
9. Chandry PS, Moore SC, Boyce JD, Davidson BE, Hillier AJ. 1997. Analysis of the DNA sequence, gene expression, origin of replication and modular structure of the Lactococcus lactis lytic bacteriophage sk1. Mol. Microbiol. 26:49-64.
10. Cheng X, Wang W, Molineux IJ. 2004. F exclusion of bacteriophage T7 occurs at the cell membrane. Virology 326:340-352.
11. Chopin A, Chopin M-C, Moillobatt A, Langella P. 1984. Two plasmiddetermined restriction and modification systems in Streptococcus lactis. Plasmid 11:260-263.
12. Chopin M-C, Chopin A, Bidnenko E. 2005. Phage abortive infection in lactococci: variations on a theme. Curr. Opin. Microbiol. 8:473-479.
13. Chung DK, Kim JH, Batt CA. 1991. Cloning and nucleotide sequence of the major capsid protein from Lactococcus lactis ssp. cremoris bacteriophage F4-1. Gene 101:121-125.
14. Clamp M, Cuff J, Searle SM, Barton GJ. 2004. The Jalview Java alignment editor. Bioinformatics 20:426-427.
15. Conway JF, et al. 2007. A thermally induced phase transition in a viral capsid transforms the hexamers, leaving the pentamers unchanged. J. Struct. Biol. 158:224-232.
16. Crutz-Le Coq AM, Cesselin B, Commissaire J, Anba J. 2002. Sequence analysis of the lactococcal bacteriophage bIL170: insights into structural proteins and HNH endonucleases in dairy phages. Microbiology 148:985-1001.
17. de Ruyter PG, Kuipers OP, de Vos WM. 1996. Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl. Environ. Microbiol. 62:3662-3667.
18. Deveau H, Garneau JE, Moineau S. 2010. CRISPR/Cas system and its role in phage-bacteria interactions. Annu. Rev. Microbiol. 64:475-493.
19. De Vos WM. 1987. Gene cloning and expression in lactic streptococci. FEMS Microbiol. Rev. 46:281-295.
20. Duda RL, Martincic K, Hendrix RW. 1995. Genetic-basis of bacteriophage HK97 prohead assembly. J. Mol. Biol. 247:636-647.
21. Émond É, et al. 1997. Phenotypic and genetic characterization of the bacteriophage abortive infection mechanism AbiK from Lactococcus lactis. Appl. Environ. Microbiol. 63:1274-1283.
22. Émond É, Moineau S. 2007. Bacteriophages and food fermentation, p 93-124. In McGrath S, Van Sinderen D (ed), Bacteriophage: genetics and molecular biology. Caister Academic Press, Norfolk, United Kingdom.
23. Fortier LC, Bransi A, 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.
24. Garcia LR, Molineux IJ. 1995. Incomplete entry of bacteriophage T7 DNA into F-plasmid containing Escherichia coli. J. Bacteriol. 177:4077-4083.
25. Garcia P, Ladero V, Suarez JE. 2003. Analysis of the morphogenetic cluster and genome of the temperate Lactobacillus casei bacteriophage A2. Arch. Virol. 148:1051-1070.
26. Garneau JE, Tremblay DM, Moineau S. 2008. Characterization of 1706, a virulent phage from Lactococcus lactis with similarities to prophages from other Firmicutes. Virology 373:298-309.
27. Gasson MJ. 1983. Plasmid complements of Streptococcus lactis NCDO-712 and other lactic streptococci after protoplast induced curing. J. Bacteriol. 154:1-9.
28. Haaber J, Moineau S, Fortier L-C, Hammer K. 2008. AbiV, a novel antiphage abortive infection mechanism on the chromosome of Lactococcus lactis subsp. cremoris MG1363. Appl. Environ. Microbiol. 74:6528-6537.
29. Haaber J, Rousseau GM, Hammer K, Moineau S. 2009. Identification and characterization of the phage gene sav, involved in sensitivity to the lactococcal abortive infection mechanism AbiV. Appl. Environ. Microbiol. 75:2484-2494.
30. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
31. Hickman AB, et al. 2005. Molecular architecture of a eukaryotic DNA transposase. Nat. Struct. Mol. Biol. 12:715-721.
32. Holo H, Nes IF. 1989. High frequency transformation, by electroporation, of Lactococcus lactis subsp. cremoris grown with glycine in osmotically stabilized media. Appl. Environ. Microbiol. 55:3119-3123.
33. Josephsen J, et al. 1994. An ecological study of lytic bacteriophages of Lactococcus lactis subsp. cremoris isolated in a cheese plant over a five year period. Int. Dairy J. 4:123-140.
34. Kim JH, Batt CA. 1991. Molecular characterization of a Lactococcus lactis bacteriophage F4-1. Food Microbiol. 8:15-26.
35. Kim JH, Batt CA. 1991. Nucleotide sequence and deletion analysis of a gene coding for a structural protein of Lactococcus lactis bacteriophage F4-1. Food Microbiol. 8:27-36.
36. Kuipers OP, de Ruyter PGGA, Kleerebezem M, de Vos WM. 1998. Quorum sensing-controlled gene expression in lactic acid bacteria. J. Biotechnol. 64:15-21.
37. Labrie S, Moineau S. 2002. Complete genomic sequence of bacteriophage ul36: demonstration of phage heterogeneity within the P335 quasi-species of lactococcal phages. Virology 296:308-320.
38. Labrie SJ, Josephsen J, Neve H, Vogensen FK, Moineau S. 2008. Morphology, genome sequence, and structural proteome of type phage P335 from Lactococcus lactis. Appl. Environ. Microbiol. 74:4636-4644.
39. Labrie SJ, Moineau S. 2007. Abortive infection mechanisms and prophage sequences significantly influence the genetic makeup of emerging lytic lactococcal phages. J. Bacteriol. 189:1482-1487.
40. Labrie SJ, Samson JE, Moineau S. 2010. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8:317-327.
41. Larkin MA, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
42. Letunic I, et al. 2006. SMART 5: domains in the context of genomes and networks. Nucleic Acids Res. 34:D257-D260. doi:10.1093/nar/gkj079.
43. Lévesque C, et al. 2005. Genomic organization and molecular analysis of virulent bacteriophage 2972 infecting an exopolysaccharide-producing Streptococcus thermophilus strain. Appl. Environ. Microbiol. 71:4057-4068.
44. Loof M, Lembke J, Teuber M. 1983. Characterization of the genome of the Streptococcus lactis "subsp. diacetylactis" bacteriophage P008 widespread in German cheese factories. Syst. Appl. Microbiol. 4:413-423.
45. Mahony J, et al. 2006. Sequence and comparative genomic analysis of lactococcal bacteriophages jj50, 712 and P008: evolutionary insights into the 936 phage species. FEMS Microbiol. Lett. 261:253-261.
46. Marchler-Bauer A, et al. 2007. CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res. 35:D237-D240. doi:10.1093/nar/gkl951.
47. McKay LL, Baldwin KA. 1984. Conjugative 40-megadalton plasmid in Streptococcus lactis subsp. diacetylactis DRC3 is associated with resistance to nisin and bacteriophage. Appl. Environ. Microbiol. 47:68-74.
48. Moineau S, Fortier J, Ackermann H-W, Pandian S. 1992. Characterization of lactococcal bacteriophages from Québec cheese plants. Can. J. Microbiol. 38:875-882.
49. Moineau S, Pandian S, Klaenhammer TR. 1994. Evolution of a lytic bacteriophage via DNA acquisition from the Lactococcus lactis chromosome. Appl. Environ. Microbiol. 60:1832-1841.
50. Moineau S, Walker S, Vedamuthu E, Vandenbergh P. 1995. Cloning and sequencing of LlaII restriction/modification genes from Lactococcus lactis and relatedness of this system to the Streptococcus pneumoniae DpnII system. Appl. Environ. Microbiol. 61:2193-2202. (Erratum, 61:3514.)
51. Molineux IJ. 1991. Host-parasite interactions: recent developments in the genetics of abortive phage infections. New Biol. 3:230-236.
52. Pesavento J, Crawford S, Estes M, Venkataram Prasad B. 2006. Rotavirus proteins: structure and assembly, p 189-219. In Roy P (ed), Reoviruses: entry, assembly and morphogenesis. Springer, Berlin, Germany.
53. Ploquin M, et al. 2008. Functional and structural basis for a bacteriophage homolog of human RAD52. Curr. Biol. 18:1142-1146.
54. Popa MP, McKelvey TA, Hempel J, Hendrix RW. 1991. Bacteriophage-HK97 structure-wholesale covalent cross-linking between the major head shell subunits. J. Virol. 65:3227-3237.
55. Rousseau GM, Moineau S. 2009. Evolution of Lactococcus lactis phages within a cheese factory. Appl. Environ. Microbiol. 75:5336-5344.
56. Samson JE, Moineau S. 2010. Characterization of Lactococcus lactis phage 949 and comparison with other lactococcal phages. Appl. Environ. Microbiol. 76:6843-6852.
57. Scaltriti E, et al. 2009. Structure and function of phage p2 ORF34(p2), a new type of single-stranded DNA binding protein. Mol. Microbiol. 73: 1156-1170.
58. Sciara G, et al. 2010. Structure of lactococcal phage p2 baseplate and its mechanism of activation. Proc. Natl. Acad. Sci. U. S. A. 107:6852-6857.
59. Staden R. 1996. The Staden sequence analysis package. Mol. Biotechnol. 5:233-241.
60. Terzaghi BE, Sandine WE. 1975. Improved medium for lactic streptococci and their bacteriophages. Appl. Microbiol. 29:807-813.
61. Veesler D, Johnson JE. 2012. Virus maturation. Annu. Rev. Biophys. 41:473-496.
62. Wells JM, Wilson PW, Le Page RW. 1993. Improved cloning vectors and transformation procedure for Lactococcus lactis. J. Appl. Bacteriol. 74: 629-636.
63. Wiedenheft B, Sternberg SH, Doudna JA. 2012. RNA-guided genetic silencing systems in bacteria and archaea. Nature 482:331-338.
64. Xie ZH, Hendrix RW. 1995. Assembly in-vitro of bacteriophage HK97 proheads. J. Mol. Biol. 253:74-85.
65. Zdobnov EM, Apweiler R. 2001. InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847-848.