Genome sequence and analysis of a broad-host range lytic bacteriophage that infects the Bacillus cereus group

Virology Journal

Volumn 10, Issue , 2013, Pages

  El Arabi, Tarek F ^a,b   Griffiths, Mansel W ^b   She, Yi Min ^c   Villegas, Andre ^d   Lingohr, Erika J ^d   Kropinski, Andrew M ^b,d  

^a Ain Shams University   (Egypt)

^b UNIVERSITY OF GUELPH   (Canada)

^c HEALTH CANADA   (Canada)

^d PUBLIC HEALTH AGENCY OF CANADA   (Canada)

Author keywords

Bacillus cereus; Bacteriophage; Genome; Host range; Myoviridae; Proteome; tRNAs

Indexed keywords

AMINO ACID; DOUBLE STRANDED DNA; TRANSFER RNA;

ARTICLE; BACILLUS CEREUS; BACTERIAL GENOME; BACTERIAL VIRULENCE; BACTERIOPHAGE; ENTEROCOCCUS; GENE SEQUENCE; LACTOBACILLUS; LISTERIA; LONG TERMINAL REPEAT; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PULSED FIELD GEL ELECTROPHORESIS; SPOROGENESIS; STAPHYLOCOCCUS;

BACILLUS CEREUS; BACILLUS PHAGES; GENOME, VIRAL; HOST SPECIFICITY; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHYLOGENY; VIRAL PROTEINS;

BACILLUS (BACTERIUM); BACILLUS CEREUS; BACILLUS CEREUS GROUP; ENTEROCOCCUS; FIRMICUTES; LACTOBACILLUS; LISTERIA; MYOVIRIDAE; POSIBACTERIA; STAPHYLOCOCCUS PHAGE K;

EID: 84873349855     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-10-48     Document Type: Article

References (67)

1. Bacillus cereus and Other Bacillus spp. Griffiths MW, Pathogens and Toxins in Foods: Challenges and Interventions Washignton, DC: ASM Press, Juneja VK, Sofos JN, 2010
2. Garber KB, Anthrax (Bacillus anthracis) KGaA: Molecular Biology of. Wiley-VCH Verlag GmbH & Co 2006
3. Bacteriophages BCP1-1 and BCP8-2 require divalent cations for efficient control of Bacillus cereus in fermented foods. Bandara N, Jo J, Ryu S, Kim KP, Food Microbiol 2012 31 1 9 16 10.1016/j.fm.2012.02.003 22475937
4. Bacillus cereus, a volatile human pathogen. Bottone EJ, Clin Microbiol Rev 2010 23 382 398 10.1128/CMR.00073-09 20375358
5. Prevalence of Bacillus cereus bacteriophages in fermented foods and characterization of phage JBP901. Shin H, Bandara N, Shin E, Ryu S, Kim KP, Res Microbiol 2011 162 8 791 797 10.1016/j.resmic.2011.07.001 21810470
6. Pathogenic potential of fifty Bacillus weihenstephanensis strains. Stenfors L, Mayr R, Scherer S, Granum P, FEMS Microbiol Lett 2002 215 47 51 10.1111/j.1574-6968.2002.tb11368.x 12393199 (Pubitemid 35232581)
7. Sub-chronic lung inflammation after airway exposures to Bacillus thuringiensis biopesticides in mice. Barfod K, Poulsen S, Hammer M, Larsen S, BMC Microbiol 2010 10 233 10.1186/1471-2180-10-233 20815884
8. Detection of toxigenic Bacillus cereus and Bacillus thuringiensis spores in U.S. rice. Int. J. Ankolekar C, Rahmati T, Labbé RG, Food Microbiol 2009 128 460 466 10.1016/j.ijfoodmicro.2008.10.006
9. Identification of Bacillus cereus group species associated with food poisoning outbreaks in British Columbia. McIntyre L, Bernard K, Beniac D, Isaac-Renton JL, Naseby DC, Canada Appl Environ Microbiol 2008 74 7451 7453 10.1128/AEM.01284-08 (Pubitemid 352773576)
10. The occurrence of Bacillus cereus, B. thuringiensis and B. mycoides in Chinese pasteurized full fat milk. Zhou G, Liu H, He J, Yuan Y, Yuan Z, Int J Food Microbiol 2008 121 195 200 10.1016/j.ijfoodmicro.2007.11.028 18077041
11. Occurrence of psychrotolerant Bacillus cereus group strains in ice creams. Zhou G, Zheng D, Dou L, Cai Q, Yuan Z, Int J Food Microbiol 2010 137 143 146 10.1016/j.ijfoodmicro.2009.12.005 20036024
12. Ackermann HW, Abedon ST, 2000 http://www.mansfield.ohio-state.edu/ ∼sabedon/names/2000/
13. New Bacillus bacteriophage species. Ackermann HW, Azizbekyan RR, Emadi Konjin HP, Lecadet MM, Seldin L, Yu MX, Arch Virol 1994 135 333 344 10.1007/BF01310018 7979971 (Pubitemid 2068544)
14. Phage Classification and Characterization. Ackermann HW, Methods Mol Biol 2009 501 127 140 10.1007/978-1-60327-164-6-13 19066817
15. Characterization of the genome of Pseudomonas aeruginosa bacteriophage PLS27 with particular reference to the ends of the DNA. Allan BJ, Davies P, Carstens EB, Kropinski AM, J Virol 1989 63 1587 1594 2494359 (Pubitemid 19085971)
16. Classification of Myoviridae bacteriophages using protein sequence similarity. Lavigne R, Darius Pl, Summer E, Seto D, Mahadevan P, Nilsson A, Ackermann H, Kropinski A, BMC Microbiol 2009 9 224 10.1186/1471-2180-9-224 19857251
17. Mapping the genes in the terminal redundancy of bacteriophage SPO1 with restriction endonucleases. Perkus ME, Shub DA, J Virol 1985 56 40 48 3928902 (Pubitemid 16256853)
18. The SPO1-related bacteriophages. Klumpp J, Lavigne R, Loessner M, Ackermann HW, Arch Virol 2010 155 1547 1561 10.1007/s00705-010-0783-0 20714761
19. The Genome of Bacillus subtilis bacteriophage SPO1. Stewart CR, Casjens SR, Cresawn SG, Houtz JM, Smith AL, Ford ME, Peebles CL, Hatfull GF, Hendrix RW, Huang WM, Pedulla ML, J Mol Biol 2009 388 48 70 10.1016/j.jmb.2009.03.009 19285085
20. Isolation and characterization of a novel Enterococcus faecalis bacteriophage EF24C as a therapeutic candidate. Uchiyama J, Rashel M, Maeda Y, Takemura I, Sugihara S, Akechi K, Muraoka A, Wakiguchi H, Matsuzaki S, FEMS Microbiol Lett 2008 278 200 206 10.1111/j.1574-6968.2007.00996.x 18096017 (Pubitemid 350264582)
21. In silico and in vivo evaluation of bacteriophage EF24C, a candidate for treatment of Enterococcus faecalis infections. Uchiyama J, Rashel M, Takemura I, Wakiguchi H, Matsuzaki S, Appl Environ Microbiol 2008 74 4149 4163 10.1128/AEM.02371-07 18456848 (Pubitemid 351962441)
22. Bacteriophage P100 for control of Listeria monocytogenes in foods: Genome sequence, bioinformatic analyses, oral toxicity study, and application. Carlton RM, Noordman WH, Biswas B, de Meester ED, Loessner MJ, Regul Toxicol Pharmacol 2005 43 301 312 10.1016/j.yrtph.2005.08.005 16188359 (Pubitemid 41616396)
23. The terminally redundant, nonpermuted genome of Listeria bacteriophage A511: a model for the SPO1-like myoviruses of Gram-positive bacteria. Klumpp J, Dorscht J, Lurz R, Bielmann R, Wieland M, Zimmer M, Calendar R, Loessner MJ, J Bacteriol 2008 190 5753 5765 10.1128/JB.00461-08 18567664
24. The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Kwan T, Liu J, DuBow M, Gros P, Pelletier J, Proc Natl Acad Sci USA 2005 102 5174 5179 10.1073/pnas.0501140102 15788529
25. Complete genome sequence of Bacillus cereus bacteriophage BCP78. Lee J, Shin H, Son B, Ryu S, J Virol 2012 86 637 638 10.1128/JVI.06520-11 22158847
26. Interspecies transduction of plasmids among Bacillus anthracis, B. cereus, and B. thuringiensis. Ruhfel RE, Robillard NJ, Thorne CB, J Bacteriol 1984 157 708 711 6421798 (Pubitemid 14151547)
27. Lysogenicity and immunity to Bacillus phage. Mccloy EW, W J Gen Microbiol 1958 18 198 220
28. Prevalence of Bacillus anthracis-like organisms and bacteriophages in the intestinal tract of the earthworm Eisenia fetida. Schuch R, Pelzek AJ, Kan S, Fischetti VA, Appl Environ Microbiol 2010 76 2286 2294 10.1128/AEM.02518-09 20118353
29. Complete genome sequence of Bacillus cereus bacteriophage PBC1. Kong M, Kim M, Ryu S, J Virol 2012 86 11 6379 6380 10.1128/JVI.00706-12 22570248
30. The secret life of the anthrax agent Bacillus anthracis: bacteriophage-mediated ecological adaptations. Schuch R, Fischetti VA, PLoS One 2009 4 6532 10.1371/journal.pone.0006532 19672290
31. Transduction in Bacillus cereus and Bacillus anthracis. Thorne CB, Microbiol Mol Biol Rev 1968 32 358 361
32. Cold lability of Bacillus cereus bacteriophage CP-51. Thorne CB, Holt SC, J Virol 1974 14 1008 1012 4138063
33. Transduction in Bacillus cereus by each of two bacteriophages. Yelton DB, Thorne CB, J Bacteriol 1970 102 573 579 4986764
34. Bacillus cereus phage typing as an epidemiological tool in outbreaks of food poisoning. Ahmed R, Sankar-Mistry P, Jackson S, Ackermann HW, Kasatiya SS, J Clin Microbiol 1995 33 636 640 7751369
35. Lee W, Billington C, Hudson JA, Heinemann JA, Isolation and characterization of phages infecting Bacillus cereus Microbiol: Lett. Appl 2011
36. Three Bacillus cereus bacteriophage endolysins are unrelated but reveal high homology to cell wall hydrolases from different bacilli. Loessner MJ, Maier SK, Daubek-Puza H, Wendlinger G, Scherer S, J Bacteriol 1997 179 2845 2851 9139898 (Pubitemid 27194429)
37. Complete Genome Sequence of Cronobacter sakazakii Bacteriophage vB-CsaM-GAP161. Abbasifar RAM, Kropinski PM, Sabour HWA, Lingohr EJ, Griffiths MW, J Virol 2012 86 13806 13807 10.1128/JVI.02546-12 23166229
38. Displacements of prohead protease genes in the late operons of double-stranded-DNA bacteriophages. Liu J, Mushegian A, J Bacteriol 2004 186 4369 4375 10.1128/JB.186.13.4369-4375.2004 15205439 (Pubitemid 38802585)
39. DBTBS: a database of Bacillus subtilis promoters and transcription factors. Ishii T, Yoshida K, Terai G, Fujita Y, Nakai K, Nucl Acids Res 2001 29 278 280 10.1093/nar/29.1.278 11125112 (Pubitemid 32054468)
40. The HHpred interactive server for protein homology detection and structure prediction. Söding J, Biegert A, Lupas AN, Nucl Acids Res 33 244 W248
41. Bacteriophages: an appraisal of their role in the treatment of bacterial infections. Hanlon GW, Int J Antimicrob Agents 2007 30 118 128 17566713 (Pubitemid 46977193)
42. Kutter E, Sulakvelidze A, Bacteriophages: biology and applications Boca Raton, FL: CRC Press 2005
43. tRNAHis guanylyltransferase (THG1), a unique 3′-5′ nucleotidyl transferase, shares unexpected structural homology with canonical 5′-3′ DNA polymerases. Hyde SJ, Eckenroth BE, Smith BA, Eberley WA, Heintz NH, Jackman JE, Doublié S, Proc Natl Acad Sci USA 2010 107 20305 20310 10.1073/pnas.1010436107 21059936
44. TFAM 1.0: an online tRNA function classifier. Nucl. Tåquist H, Cui Y, Ardell DH, Acids Res 2007 35 350 W353 10.1093/nar/gkm393
45. Integration host factor (IHF) dictates the structure of polyamine-DNA condensates: implications for the role of IHF in the compaction of bacterial Chromatin. Sarkar T, Petrov AS, Vitko JR, Santai CT, Harvey SC, Mukerji I, Hud NV, Biochemistry 2009 48 667 675 10.1021/bi8019965 19132923
46. Identifying active phage lysins through functional viral metagenomics. Schmitz JE, Schuch R, Fischetti VA, Appl Environ Microbiol 2010 76 7181 7187 10.1128/AEM.00732-10 20851985
47. In silico identification of genes in bacteriophage DNA. Kropinski AM, Borodovsky M, Carver TJ, Cerdeño-Tárraga AM, Darling A, Lomsadze A, Mahadevan P, Stothard P, Seto D, Domselaar G, Wishart DS, Methods Mol Biol 2009 502 57 89 10.1007/978-1-60327-565-1-6 19082552
48. CoreGenes: A computational tool for identifying and cataloging "core" genes in a set of small genomes. Zafar N, Mazumder R, Seto D, BMC Bioinforma 2002 3 12 10.1186/1471-2105-3-12 (Pubitemid 38751192)
49. Genomics of staphylococcal Twort-like phages-potential therapeutics of the post-antibiotic era. Łobocka M, Hejnowicz MS, Da̧browski K, Gozdek A, Kosakowski J, Witkowska M, Ulatowska MI, Weber-Da̧browska B, Kwiatek M, Parasion S, Gawor J, Kosowska H, Głowacka A, Adv Virus Res 2012 83 143 216 22748811
50. A feeding tube model for activation of a cell-specific transcription factor during sporulation in Bacillus subtilis. Camp AH, Losick R, Genes Dev 2009 23 1014 1024 10.1101/gad.1781709 19390092
51. Postseptational chromosome partitioning in bacteria. Sharpe ME, Errington J, Proc Natl Acad Sci USA 1995 92 8630 8634 10.1073/pnas.92.19.8630 7567988
52. Use of asymmetric cell division and spoIIIE mutants to probe chromosome orientation and organization in Bacillus subtilis. Wu LJ, Errington J, Molec Microbiol 1998 27 777 786 10.1046/j.1365-2958.1998.00724.x (Pubitemid 28081986)
53. Anany HE, Biocontrol of FoodBorne Bacterial Pathogens Using Immobilized Bacteriophages University of Guelph Libraries, Ph.D. University of Guelph 2010
54. Experimental examination of bacteriophage latent-period evolution as a response to bacterial availability. Abedon S, Hyman P, Thomas C, Appl Environ Microbiol 2003 69 7499 7506 10.1128/AEM.69.12.7499-7506.2003 14660403 (Pubitemid 38585406)
55. Determination of bacteriophage genome size by pulsed-field gel electrophoresis. Lingohr E, Frost S, Johnson RP, Methods Mol Biol 2009 502 19 25 10.1007/978-1-60327-565-1-3 19082549
56. AutoFACT: An automatic functional annotation and classification tool. Koski L, Gray M, Lang BF, Burger G, BMC Bioinforma 2005 6 151 10.1186/1471-2105-6-151 (Pubitemid 41357996)
57. The Pfam protein families database. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer ELL, Eddy SR, Bateman A, Nucl Acids Res 2010 38 211 D222 10.1093/nar/gkp985 19920124
58. ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Laslett D, Canback B, Nucl Acids Res 2004 32 11 16 10.1093/nar/gkh152 14704338 (Pubitemid 38228599)
59. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Lowe TM, Eddy SR, Nucl Acids Res 1997 25 955 964 9023104 (Pubitemid 27298263)
60. Prediction of transcription terminators in bacterial genomes. Ermolaeva MD, Khalak HG, White O, Smith HO, Salzberg SL, J Mol Biol 2000 301 27 33 10.1006/jmbi.2000.3836 10926490
61. Direct RNA motif definition and identification from multiple sequence alignments using secondary structure profiles. Gautheret D, Lambert A, J Mol Biol 2001 313 1003 1011 10.1006/jmbi.2001.5102 11700055 (Pubitemid 33081896)
62. Mfold web server for nucleic acid folding and hybridization prediction. Zuker M, Nucl Acids Res 2003 31 3406 3415 10.1093/nar/gkg595 12824337 (Pubitemid 37442169)
63. Basic charge clusters and predictions of membrane protein topology. Juretić D, Zoranić L, Zucić D, J Chem Inf Comput Sci 2002 42 620 632 10.1021/ci010263s 12086524 (Pubitemid 35355271)
64. Advantages of combined transmembrane topology and signal peptide prediction-the Phobius web server. Käll L, Krogh A, Sonnhammer ELL, Nucl Acids 2007 35 429 432 10.1093/nar/gkm256
65. Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL, J Mol Biol 2001 305 567 580 10.1006/jmbi.2000.4315 11152613 (Pubitemid 33032862)
66. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. Darling AE, Mau B, Perna NT, PLoS One 2010 5 11147 10.1371/journal.pone.0011147 20593022
67. Circular genome visualization and exploration using CGView. Stothard P, Wishart DS, Bioinformatics 2005 21 537 539 10.1093/bioinformatics/bti054 15479716 (Pubitemid 40310241)