Genome of enterobacteriophage lula/phi80 and insights into its ability to spread in the laboratory environment

Journal of Bacteriology

Volumn 194, Issue 24, 2012, Pages 6802-6817

  Rotman, Ella ^a   Kouzminova, Elena ^a   Plunkett, Guy ^b,c   Kuzminov, Andrei ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c DNASTAR Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; DNA ADENINE METHYLTRANSFERASE;

ARTICLE; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL GENOME; BACTERIOPHAGE; BACTERIOPHAGE LULA; BACTERIUM CONTAMINATION; BACTERIUM CULTURE; CONTROLLED STUDY; DNA DAMAGE; DNA MODIFICATION; ESCHERICHIA COLI; GENE DELETION; GENE DOSAGE; GENE MUTATION; GENE SEQUENCE; LABORATORY; NONHUMAN; PRIORITY JOURNAL;

EID: 84870664508     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/jb.01353-12     Document Type: Article

References (95)

1. Abraham ZH, Symonds N. 1990. Purification of overexpressed gam gene protein from bacteriophage Mu by denaturation-renaturation techniques and a study of its DNA-binding properties. Biochem. J. 269:679-684.
2. Aizawa S, Matsushiro A. 1975. Studies on temperature sensitive growth of phage phi80. I. Prophage excision. Virology 67:168-178.
3. Akroyd JE, Clayson E, Higgins NP. 1986. Purification of the gam geneproduct of bacteriophage Mu and determination of the nucleotide sequence of the gam gene. Nucleic Acids Res. 14:6901-6914.
4. Amundsen SK, Neiman AM, Thibodeaux SM, Smith GR. 1990. Genetic dissection of the biochemical activities of RecBCD enzyme. Genetics 126: 25-40.
5. Bachmann BJ. 1987. Derivations and genotypes of some mutant derivatives of Escherichia coli K-12, p 1190-1219. In Neidhardt FC et al (ed), Escherichia coli and Salmonella typhimurium: cellular and molecular biology. American Society for Microbiology, Washington, DC.
6. Bethesda Research Laboratories. 1986. BRL pUC host: E. coli DH5 competent cells. Focus 8:9.
7. Campbell A. 1994. Comparative molecular biology of lamboid phages. Annu. Rev. Microbiol. 48:193-222.
8. Carlson K, Miller ES. 1994. Working with T4, p 421-426. In Karam JD (ed), Molecular biology of bacteriophage T4. ASM Press, Washington, DC.
9. Carlson K, Raleigh EA, Hattman S. 1994. Restriction and modification, p 369-381. In Karam JD (ed), Molecular biology of bacteriophage T4. ASM Press, Washington, DC.
10. Casjens SR, et al. 2004. The pKO2 linear plasmid prophage of Klebsiella oxytoca. J. Bacteriol. 186:1818-1832.
11. Chalker AF, Leach DRF, Lloyd RG. 1988. Escherichia coli sbcC mutants permit stable propagation of DNA replicons containing a long palindrome. Gene 71:201-205.
12. Clark AJ, Inwood W, Cloutier T, Dhillon TS. 2001. Nucleotide sequence of coliphage HK620 and the evolution of lambdoid phages. J. Mol. Biol. 311:657-679.
13. Cohen PT, Cohen P. 1989. Discovery of a protein phosphatase activity encoded in the genome of bacteriophage lambda. Probable identity with open reading frame 221. Biochem. J. 260:931-934.
14. Cohen PTW, Collins JF, Coulson AFW, Berndta N, and OBda Cruz e Silva. 1988. Segments of bacteriophage λ(orf221) and φ80 are homologous to genes coding for mammalian protein phosphatases. Gene 69:131-134.
15. Connelly JC, Kirkham LA, Leach DRF. 1998. The SbcCD nuclease of Escherichia coli is a structural maintenance of chromosomes (SMC) family protein that cleaves hairpin DNA. Proc. Natl. Acad. Sci. U. S. A. 95:7969-7974.
16. Connelly JC, Leach DR. 1996. The sbcC and sbcD genes of Escherichia coli encode a nuclease involved in palindrome inviability and genetic recombination. Genes Cells 1:285-291.
17. Conter A, Bouché JP, Dassain M. 1996. Identification of a new inhibitor of essential division gene ftsZ as the kil gene of defective prophage Rac. J. Bacteriol. 178:5100-5104.
18. Coulby JN, Sternberg NL. 1988. Characterization of the phage P1 dam gene. Gene 74:191.
19. Court D, Oppenheim A. 1983. Phage lambda's accessory genes, p 251-277. In Hendrix RW, Roberts JW, Stahl FW, Weisberg RA (ed), Lambda II. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
20. Court R, Cook N, Saikrishnan K, Wigley D. 2007. The crystal structure of lambda-Gam protein suggests a model for RecBCD inhibition. J. Mol. Biol. 371:25-33.
21. d'Adda di Fagagna F, Weller GR, Doherty AJ, Jackson SP. 2003. The Gam protein of bacteriophage Mu is an orthologue of eukaryotic Ku. EMBO Rep. 4:47-52.
22. Daniels DL, Schroeder JL, Szybalski W, Sanger F, Blattner FR. 1983. A molecular map of coliphage lambda, p 469-517. In Hendrix RW, Roberts JW, Stahl FW, Weisberg RA (ed), Lambda II. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
23. Daniels DL, et al. 1983. Complete annotated lambda sequence, p 519-676. In Hendrix RW, Roberts JW, Stahl FW, Weisberg RA (ed), Lambda II. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
24. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
25. Devoret R, Pierre M, Moreau PL. 1983. Prophage phi80 is induced in Escherichia coli K12 recA430. Mol. Gen. Genet. 189:199-206.
26. Dillingham MS, Kowalczykowski SC. 2008. RecBCD enzyme and the repair of double-strandedDNAbreaks. Microbiol. Mol. Biol. Rev. 72:642-671.
27. Durfee T, et al. 2008. The complete genome sequence of Escherichia coli DH10B: insights into the biology of a laboratory workhorse. J. Bacteriol. 190:2597-2606.
28. Eguchi Y, Ogawa T, Ogawa H. 1988. Cleavage of bacteriophage phi80 cI repressor by RecA protein. J. Mol. Biol. 202:565-573.
29. Endriss F, Braun V. 2004. Loop deletions indicate regions important for FhuA transport and receptor functions in Escherichia coli. J. Bacteriol. 186:4818-4823.
30. Enquist LW, Skalka A. 1973. Replication of bacteriophage l DNA dependent on the function of host and viral genes. I. Interaction of red, gam, and rec. J. Mol. Biol. 75:185-212.
31. Fernández de Henestrosa AR, et al. 2000. Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol. Microbiol. 35:1560-1572.
32. Fiandt M, Hradecna Z, Lozeron HA, Szybalski W. 1971. Electron micrographic mapping of deletions, insertions, inversions and homologies in the DNAs of coliphages lambda and Phi 80, p 329-354. In Hershey AD (ed), The bacteriophage lambda. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
33. Fineran PC, et al. 2009. The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc. Nat. Acad. Sci. U. S. A. 106:894-899.
34. Friedman SA, Hays JB. 1986. Selective inhibition of Escherichia coli RecBC activities by plasmid-encoded GamS function of phage lambda. Gene 43:255-263.
35. Gunn JS, Alpuche-Aranda CM, Loomis WP, Belden WJ, Miller SI. 1995. Characterization of the Salmonella typhimurium pagC/pagD chromosomal region. J. Bacteriol. 177:5040-5047.
36. Hancock RW, Braun V. 1976. Nature of the energy requirement for the irreversible adsorption of bacteriophages T1 and phi80 to Escherichia coli. J. Bacteriol. 125:409-415.
37. Hay RJ. 1991. Operator-induced contamination in cell culture systems. Dev. Biol. Stand. 75:193-204.
38. Henderson D, Weil J. 1975. Recombination deficient deletions in bacteriophage λ and their interaction with chi mutations. Genetics 79:143-174.
39. Hughes P, Marshall D, Reid Y, Parkes H, Gelber C. 2007. The costs of using unauthenticated, over-passaged cell lines: how much more data do we need? Biotechniques 43:575-584.
40. Ingraham J. 1987. Effect of temperature, pH, water activity, and pressure on growth, p 1543-1554. In Neidhardt FC, et al (ed), Escherichia coli and Salmonella typhimurium: cellular and molecular biology. American Society for Microbiology, Washington, DC.
41. Juhala RJ, et al. 2000. Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J. Mol. Biol. 299:27-51.
42. Kadner RJ, Heller K, Coulton JW, Braun V. 1980. Genetic control of hydroxamate-mediated iron uptake in Escherichia coli. J. Bacteriol. 143: 256-264.
43. Karu AE, Sakaki Y, Echols H, Linn S. 1975. The gamma protein specified by bacteriophage lambda. Structure and inhibitory activity for the recBC enzyme of Escherichia coli. J. Biol. Chem. 250:7377-7387.
44. King G, Murray NE. 1995. Restriction alleviation and modification enhancement by the Rac prophage of Escherichia coli K-12. Mol. Microbiol. 16:769-777.
45. Kouzminova EA, Kuzminov A. 2004. Chromosomal fragmentation in dUTPase-deficient mutants of Escherichia coli and its recombinational repair. Mol. Microbiol. 51:1279-1295.
46. Kroger M, Hobom G. 1982. A chain of interlinked genes in the ninR region of bacteriophage lambda. Gene 20:25-38.
47. Kulkarni SK, Stahl FW. 1989. Interaction between the sbcC gene of Escherichia coli and gam gene of phage lambda. Genetics 123:249-253.
48. Langdon SP. 2004. Cell culture contamination: an overview. Methods Mol. Med. 88:309-317.
49. Larsen RA, Wilson MM, Guss AM, Metcalf WW. 2002. Genetic analysis of pigment biosynthesis in Xanthobacter autotrophicus Py2 using a new, highly efficient transposon mutagenesis system that is functional in a wide variety of bacteria. Arch. Microbiol. 178:193-201.
50. Lewis K. 2010. Persister cells. Annu. Rev. Microbiol. 64:357-372.
51. Lewis LK, Harlow GR, Gregg-Jolly LA, Mount DW. 1994. Identification of high affinity binding sites for LexA which define new DNA damageinducible genes in Escherichia coli. J. Mol. Biol. 241:507-523.
52. Lipinska B, Rao AS, Bolten BM, Balakrishnan R, Goldberg EB. 1989. Cloning and identification of bacteriophage T4 gene 2 product gp2 and action of gp2 on infecting DNA in vivo. J. Bacteriol. 171:488-497.
53. Little JW. 1983. The SOS regulatory system: control of its state by the level of RecA protease. J. Mol. Biol. 167:791-808.
54. Little JW, Edmiston SH, Pacelli LZ, Mount DW. 1980. Cleavage of the Escherichia coli LexA protein by the RecA protease. Proc. Natl. Acad. Sci. U. S. A. 77:3225-3229.
55. Little JW, Mount DW. 1982. The SOS regulatory system of Escherichia coli. Cell 29:11-22.
56. Łobocka MB, et al. 2004. Genome of bacteriophage P1. J. Bacteriol. 186:7032-7068.
57. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acid Res. 25: 955-964.
58. Lozeron HA, Szybalski W. 1969. Congruent transcriptional controls and heterology of base sequences in coliphages lambda and phi80. Virology 39:373-388.
59. Lusetti SL, Drees JC, Stohl EA, Seifert HS, Cox MM. 2004. The DinI and RecX proteins are competing modulators of RecA function. J. Biol. Chem. 279:55073-55079.
60. Lusetti SL, Voloshin ON, Inman RB, Camerini-Otero RD, Cox MM. 2004. The DinI protein stabilizes RecA protein filaments. J. Biol. Chem. 279:30037-30046.
61. Marinus MG, Morris NR. 1975. Pleiotropic effects of a DNA adenine methylation mutation (dam-3) in Escherichia coli K12. Mutat. Res. 28:15-26.
62. Marsic N, Roje S, Stojiljcovic I, Salaj-Smic E, Trgovcevic Z. 1993. In vivo studies on the interaction of RecBCD enzyme and lambda Gam protein. J. Bacteriol. 175:4738-4743.
63. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
64. Morita T, Ichikawa N, Yamaguchi T, Matsushiro A. 1983. Isolation and characterization of deletion mutants affected in early genes of bacteriophage phi80 Mol. Gen. Genet. 183:144-151.
65. Mount DW, Low KB, Edmiston SJ. 1972. Dominant mutations (lex) in Escherichia coli K-12 which affect radiation sensitivity and frequency of ultraviolet light-induced mutations. J. Bacteriol. 112:886-893.
66. Murphy KC. 1991. λGam protein inhibits the helicase and Χ-stimulated recombination activities of Escherichia coli RecBCD enzyme. J. Bacteriol. 173:5808-5821.
67. Ogawa T, Ogawa H, Tomizawa J. 1988. Organization of the early region of bacteriophage phi 80. Genes and proteins. J. Mol. Biol. 202:537-550.
68. Oppenheim AB, Kobiler O, Stavans J, Court DL, Adhya S. 2005. Switches in bacteriophage lambda development. Annu. Rev. Genet. 39: 409-429.
69. Parma DH, et al. 1992. The Rex system of bacteriophage lambda: tolerance and altruistic cell death. Genes Dev. 6:497-510.
70. Peterson KR, Wertman KF, Mount DW, Marinus MG. 1985. Viability of Escherichia coli K-12 DNA adenine methylase (dam) mutants requires increased expression of specific genes in the SOS regulon. Mol. Gen. Genet. 201:14-19.
71. Phizicky EM, Roberts JW. 1981. Induction of SOS functions: regulation of proteolytic activity of E. coli RecA protein by interaction with DNA and nucleoside triphosphate. Cell 25:259-267.
72. Plunkett G, III, Rose DJ, Durfee TJ, Blattner FR. 1999. Sequence of Shiga toxin 2 phage 933W from Escherichia coli O157:H7: Shiga toxin as a phage late-gene product. J. Bacteriol. 181:1767-1778.
73. Ravin NV. 2011. N15: the linear phage-plasmid. Plasmid 65:102-109.
74. Renzette N, Gumlaw N, Sandler SJ. 2007. DinI and RecX modulate RecA-DNA structures in Escherichia coli K-12. Mol. Microbiol. 63:103-115.74.
75. Rotman E, Amado L, Kuzminov A. 2010. Unauthorized horizontal spread in the laboratory environment: the tactics of Lula, a temperate lambdoid bacteriophage of Escherichia coli. PLoS One 5:e11106. doi:10.1371/journal.pone.0011106.
76. Rottem S, Barile MF. 1993. Beware of mycoplasmas. Trends Biotechnol. 11:143-151.
77. Rybchin VN. 1984. Genetics of bacteriophage phi80-a review. Gene 27:3-11.
78. Sakaki Y. 1974. Inactivation of the ATP-dependent DNase of Escherichia coli after infection with double-stranded DNA phages. J. Virol. 14:1611-1612.
79. Scherzer E, Auer B, Schweiger M. 1987. Identification, purification, and characterization of Escherichia coli virus T1 DNA methyltransferase. J. Biol. Chem. 262:15225-15231.
80. Segawa T, Inokuchi I, Ozeki H. 1973. Genetic study on temperature sensitive nature of phage φ80. Virology 54:287-289.
81. Sergueev K, Yu D, Austin S, Court D. 2001. Cell toxicity caused by products of the p(L) operon of bacteriophage lambda. Gene 272:227-235.
82. Sharples GJ, Leach DRF. 1995. Structural and functional similarities between the SbcCD proteins of Escherichia coli and the RAD50 and MRE11 (RAD32) recombination and repair proteins of yeast. Mol. Microbiol. 17:1215-1220.
83. Shinedling S, Parma D, Gold L. 1987. Wild-type bacteriophage T4 is restricted by the lambda rex genes. J. Virol. 61:3790-3794.
84. Signer ER, Beckwith JR. 1966. Transposition of the lac region of Escherichia coli. III. The mechanism of attachment of bacteriophage ψ80 to the bacterial chromosome. J. Mol. Biol. 22:33-51.
85. Silverstein JL, Goldberg EB. 1976. T4 DNA injection. II. Protection of entering DNA from host exonuclease V. Virology 72:212-223.
86. Simon MN, Davis RW, Davidson N. 1971. Heteroduplexes of DNA molecules of lambdoid phages: physical mapping of their base sequence relationships by electron microscopy, p 313-328. In HersheyAD(ed), The bacteriophage lambda. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
87. Takayama KM, Houba-Herin N, Inouye M. 1987. Overproduction of an antisense RNA containing the oop RNA sequence of bacteriophage lambda induces clear plaque formation. Mol. Gen. Genet. 210:184-186.
88. Tolmach LJ. 1957. Attachment and penetration of cells by viruses. Adv. Virus Res. 4:63-110.
89. Van Melderen L. 2010. Toxin-antitoxin systems: why so many, what for? Curr. Opin. Microbiol. 13:781-785.
90. Vostrov AA, Vostrukhina OA, Svarchevsky AN, Rybchin VN. 1996. Proteins responsible for lysogenic conversion caused by coliphages N15 and phi80 are highly homologous. J. Bacteriol. 178:1484-1486.
91. Wietzorrek A, Schwarz H, Herrmann C, Braun V. 2006. The genome of the novel phage Rtp, with a rosette-like tail tip, is homologous to the genome of phage T1. J. Bacteriol. 188:1419-1436.
92. Yamaguchi Y, Park JH, Inouye M. 2011. Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet. 45:61-79.
93. Yasuda T, Morimatsu K, Horii T, Nagata T, Ohmori H. 1998. Inhibition of Escherichia coli RecA coprotease activities by DinI. EMBO J. 17:3207-3216.
94. Yasuda T, et al. 2001. Physical interactions between DinI and RecA nucleoprotein filament for the regulation of SOS mutagenesis. EMBO J. 20:1192-1202.
95. Zissler J, Signer ER, Schaefer F. 1971. The role of recombination in growth of bacteriophage lambda. I. The gamma gene, p 455-468. In Hershey AD (ed), The bacteriophage lambda. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.