Archives of Virology

, Volume 159, Issue 5, pp 871–884

Characterization and comparative genomic analysis of bacteriophages infecting members of the Bacillus cereus group

Brief Review

Abstract

The Bacillus cereus group phages infecting B. cereus, B. anthracis, and B. thuringiensis (Bt) have been studied at the molecular level and, recently, at the genomic level to control the pathogens B. cereus and B. anthracis and to prevent phage contamination of the natural insect pesticide Bt. A comparative phylogenetic analysis has revealed three different major phage groups with different morphologies (Myoviridae for group I, Siphoviridae for group II, and Tectiviridae for group III), genome size (group I > group II > group III), and lifestyle (virulent for group I and temperate for group II and III). A subsequent phage genome comparison using a dot plot analysis showed that phages in each group are highly homologous, substantiating the grouping of B. cereus phages. Endolysin is a host lysis protein that contains two conserved domains: a cell-wall-binding domain (CBD) and an enzymatic activity domain (EAD). In B. cereus sensu lato phage group I, four different endolysin groups have been detected, according to combinations of two types of CBD and four types of EAD. Group I phages have two copies of tail lysins and one copy of endolysin, but the functions of the tail lysins are still unknown. In the B. cereus sensu lato phage group II, the B. anthracis phages have been studied and applied for typing and rapid detection of pathogenic host strains. In the B. cereus sensu lato phage group III, the B. thuringiensis phages Bam35 and GIL01 have been studied to understand phage entry and lytic switch regulation mechanisms. In this review, we suggest that further study of the B. cereus group phages would be useful for various phage applications, such as biocontrol, typing, and rapid detection of the pathogens B. cereus and B. anthracis and for the prevention of phage contamination of the natural insect pesticide Bt.

Supplementary material

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Supplementary material 1 (DOCX 1331 kb)

References

  1. 1.
    Abshire TG, Brown JE, Ezzell JW (2005) Production and validation of the use of gamma phage for identification of Bacillus anthracis. J Clin Microbiol 43:4780–4788PubMedCentralPubMedCrossRefGoogle Scholar
  2. 2.
    Ackermann HW, Roy R, Martin M, Murthy MRV, Smirnoff WA (1978) Partial characterization of a cubic Bacillus phage. Can J Microbiol 24:986–993PubMedCrossRefGoogle Scholar
  3. 3.
    Ackermann HW (2001) Frequency of morphological phage descriptions in the year 2000. Arch Virol 146:843–857PubMedCrossRefGoogle Scholar
  4. 4.
    Agaisse H, Lereclus D (1995) How does Bacillus thuringiensis produce so much insecticidal crystal protein? J Bacteriol 177:6027–6032PubMedCentralPubMedGoogle Scholar
  5. 5.
    Athamna A, Athamna M, Abu-Rashed N, Medlej B, Bast DJ, Rubinstein E (2004) Selection of Bacillus anthracis isolates resistant to antibiotics. J Antimicrob Chemother 54:424–428PubMedCrossRefGoogle Scholar
  6. 6.
    Bandara N, Jo J, Ryu S, Kim K-P (2012) Bacteriophages BCP1-1 and BCP8-2 require divalent cations for efficient control of Bacillus cereus in fermented foods. Food Microbiol 31:9–16PubMedCrossRefGoogle Scholar
  7. 7.
    Bartlett JG, Inglesby TV Jr, Borio L (2002) Management of anthrax. Clin Infect Dis 35:851–858PubMedCrossRefGoogle Scholar
  8. 8.
    Bishop-Lilly KA, Plaut RD, Chen PE, Akmal A, Willner KM, Butani A, Dorsey S, Mokashi V, Mateczun AJ, Chapman C, George M, Luu T, Read TD, Calendar R, Stibitz S, Sozhamannan S (2012) Whole genome sequencing of phage resistant Bacillus anthracis mutants reveals an essential role for cell surface anchoring protein CsaB in phage AP50c adsorption. Virol J 9:246PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Bottone EJ (2010) Bacillus cereus, a volatile human pathogen. Clin Microbiol Rev 23:382–398PubMedCentralPubMedCrossRefGoogle Scholar
  10. 10.
    Breitbart M, Rohwer F (2005) Here a virus, there a virus, everywhere the same virus? Trend Microbiol 13:278–284CrossRefGoogle Scholar
  11. 11.
    Brodie R, Roper RL, Upton C (2004) JDotter: a Java interface to multiple dotplots generated by dotter. Bioinformatics 20:279–281PubMedCrossRefGoogle Scholar
  12. 12.
    Brown ER, Cherry WB (1955) Specific identification of Bacillus anthracis by means of a variant bacteriophage. J Infect Dis 96:34–39PubMedCrossRefGoogle Scholar
  13. 13.
    Choudhury B, Leoff C, Saile E, Wilkins P, Quinn CP, Kannenberg EL, Carlson RW (2006) The Structure of the major cell wall polysaccharide of Bacillus anthracis is species-specific. J Biol Chem 281:27932–27941PubMedCrossRefGoogle Scholar
  14. 14.
    Daffonchio D, Cherif A, Borin S (2000) Homoduplex and heteroduplex polymorphisms of the amplified ribosomal 16S-23S internal transcribed spacers describe genetic relationships in the “Bacillus cereus group”. Appl Environ Microbiol 66:5460–5468PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Davison S, Couture-Tosi E, Candela T, Mock M, Fouet A (2005) Identification of the Bacillus anthracis gamma phage receptor. J Bacteriol 187:6742–6749PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    Dong Z, Peng D, Wang Y, Zhu L, Ruan L, Sun M (2013) Complete genome sequence of Bacillus thuringiensis bacteriophage BMBtp2. Genome Announc 1:e00011–e00012PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    El-Arabi TF, Griffiths MW, She YM, Villegas A, Lingohr EJ, Kropinski AM (2013) Genome sequence and analysis of a broad-host range lytic bacteriophage that infects the Bacillus cereus group. Virol J 10:48PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Fornelos N, Bamford JK, Mahillon J (2011) Phage-borne factors and host LexA regulate the lytic switch in phage GIL01. J Bacteriol 193:6008–6019PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Fouts DE, Rasko DA, Cer RZ, Jiang L, Fedorova NB, Shvartsbeyn A, Vamathevan JJ, Tallon L, Althoff R, Arbogast TS, Fadrosh DW, Read TD, Gill SR (2006) Sequencing Bacillus anthracis typing phages gamma and cherry reveals a common ancestry. J Bacteriol 188:3402–3408PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Gaidelyte A, Cvirkaite-Krupovic V, Daugelavicius R, Bamford JK, Bamford DH (2006) The entry mechanism of membrane-containing phage Bam35 infecting Bacillus thuringiensis. J Bacteriol 188:5925–5934PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.
    Granum PE, Lund T (1997) Bacillus cereus and its food poisoning toxins. FEMS Microbiol Lett 157:223–228PubMedCrossRefGoogle Scholar
  22. 22.
    Greenfield RA, Bronze MS (2003) Prevention and treatment of bacterial diseases caused by bacterial bioterrorism threat agents. Drug Discov Today 8:881–888PubMedCrossRefGoogle Scholar
  23. 23.
    Hardies SC, Thomas JA, Serwer P (2007) Comparative genomics of Bacillus thuringiensis phage 0305 phi 8-36: defining patterns of descent in a novel ancient phage lineage. Virol J 4:97PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Helgason E, Okstad OA, Caugant DA, Johansen HA, Fouet A, Mock M, Hegna I, Kolsto AB (2000) Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis–one species on the basis of genetic evidence. Appl Environ Microbiol 66:2627–2630PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Hendrix RW (2003) Bacteriophage genomics. Curr Opin Microbiol 6:506–511PubMedCrossRefGoogle Scholar
  26. 26.
    King AMQ, International Committee on Taxonomy of Viruses (2012) Virus taxonomy: classification and nomenclature of viruses: ninth report of the International Committee on Taxonomy of Viruses. Academic Press, LondonGoogle Scholar
  27. 27.
    Ivanova N, Sorokin A, Anderson I, Galleron N, Candelon B, Kapatral V, Bhattacharyya A, Reznik G, Mikhailova N, Lapidus A, Chu L, Mazur M, Goltsman E, Larsen N, D’Souza M, Walunas T, Grechkin Y, Pusch G, Haselkorn R, Fonstein M, Ehrlich SD, Overbeek R, Kyrpides N (2003) Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423:87–91PubMedCrossRefGoogle Scholar
  28. 28.
    Jensen GB, Hansen BM, Eilenberg J, Mahillon J (2003) The hidden lifestyles of Bacillus cereus and relatives. Environ Microbiol 5:631–640PubMedCrossRefGoogle Scholar
  29. 29.
    Kikkawa H, Fujinami Y, Suzuki S, Yasuda J (2007) Identification of the amino acid residues critical for specific binding of the bacteriolytic enzyme of gamma-phage, PlyG, to Bacillus anthracis. Biochem Biophys Res Commun 363:531–535PubMedCrossRefGoogle Scholar
  30. 30.
    Kikkawa HS, Ueda T, Suzuki S, Yasuda J (2008) Characterization of the catalytic activity of the gamma-phage lysin, PlyG, specific for Bacillus anthracis. FEMS Microbiol Lett 286:236–240PubMedCrossRefGoogle Scholar
  31. 31.
    Kiyomizu K, Yagi T, Yoshida H, Minami R, Tanimura A, Karasuno T, Hiraoka A (2008) Fulminant septicemia of Bacillus cereus resistant to carbapenem in a patient with biphenotypic acute leukemia. J Infect Chemother 14:361–367PubMedCrossRefGoogle Scholar
  32. 32.
    Kong M, Kim M, Ryu S (2012) Complete genome sequence of Bacillus cereus bacteriophage PBC1. J Virol 86:6379–6380PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinf 9:299–306CrossRefGoogle Scholar
  34. 34.
    Kutter E, Sulakvelidze A (2005) Bacteriophages: biology and applications. CRC Press, Boca RatonGoogle Scholar
  35. 35.
    Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948PubMedCrossRefGoogle Scholar
  36. 36.
    Lavigne R, Darius P, Summer EJ, Seto D, Mahadevan P, Nilsson AS, Ackermann HW, Kropinski AM (2009) Classification of Myoviridae bacteriophages using protein sequence similarity. BMC Microbiol 9:224PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Lee JH, Shin H, Son B, Ryu S (2012) Complete genome sequence of Bacillus cereus bacteriophage BCP78. J Virol 86:637–638PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Lee JH, Shin H, Son B, Heu S, Ryu S (2013) Characterization and complete genome sequence of a virulent bacteriophage B4 infecting food-borne pathogenic Bacillus cereus. Arch Virol. doi:10.1007/s00705-013-1719-2 Google Scholar
  39. 39.
    Lee WJ, Billington C, Hudson JA, Heinemann JA (2011) Isolation and characterization of phages infecting Bacillus cereus. Lett Appl Microbiol 52:456–464PubMedCrossRefGoogle Scholar
  40. 40.
    Lee YD, Park JH (2012) Genome organization of temperate phage 11143 from emetic Bacillus cereus NCTC11143. J Microbiol Biotechnol 22:649–653PubMedCrossRefGoogle Scholar
  41. 41.
    Liao W, Song S, Sun F, Jia Y, Zeng W, Pang Y (2008) Isolation, characterization and genome sequencing of phage MZTP02 from Bacillus thuringiensis MZ1. Arch Virol 153:1855–1865PubMedCrossRefGoogle Scholar
  42. 42.
    Loessner MJ, Maier SK, Daubek-Puza H, Wendlinger G, Scherer S (1997) Three Bacillus cereus bacteriophage endolysins are unrelated but reveal high homology to cell wall hydrolases from different bacilli. J Bacteriol 179:2845–2851PubMedCentralPubMedGoogle Scholar
  43. 43.
    McGrath S, van Sinderen D (2007) Bacteriophage: genetics and molecular biology. Caister Academic Press, Norfolk, EnglandGoogle Scholar
  44. 44.
    McNair K, Bailey BA, Edwards RA (2012) PHACTS, a computational approach to classifying the lifestyle of phages. Bioinformatics 28:614–618PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Minakhin L, Semenova E, Liu J, Vasilov A, Severinova E, Gabisonia T, Inman R, Mushegian A, Severinov K (2005) Genome sequence and gene expression of Bacillus anthracis bacteriophage Fah. J Mol Biol 354:1–15PubMedCrossRefGoogle Scholar
  46. 46.
    Moumen B, Nguen-The C, Sorokin A (2012) Sequence analysis of inducible prophage phIS3501 integrated into the haemolysin II gene of Bacillus thuringiensis var. israelensis ATCC35646. Genet Res Int 2012:543286Google Scholar
  47. 47.
    Nagy E (1974) A highly specific phage attacking Bacillus anthracis strain Sterne. Acta Microbiol Acad Sci Hung 21:257PubMedGoogle Scholar
  48. 48.
    Oakley BB, Talundzic E, Morales CA, Hiett KL, Siragusa GR, Volozhantsev NV, Seal BS (2011) Comparative genomics of four closely related Clostridium perfringens bacteriophages reveals variable evolution among core genes with therapeutic potential. BMC genomics 12:282PubMedCentralPubMedCrossRefGoogle Scholar
  49. 49.
    Park J, Yun J, Lim JA, Kang DH, Ryu S (2012) Characterization of an endolysin, LysBPS13, from a Bacillus cereus bacteriophage. FEMS Microbiol Lett 332:76–83PubMedCrossRefGoogle Scholar
  50. 50.
    Reiman RW, Atchley DH, Voorhees KJ (2007) Indirect detection of Bacillus anthracis using real-time PCR to detect amplified gamma phage DNA. J Microbiol Methods 68:651–653PubMedCrossRefGoogle Scholar
  51. 51.
    Rohwer F (2003) Global phage diversity. Cell 113:141PubMedCrossRefGoogle Scholar
  52. 52.
    Sainathrao S, Mohan KV, Atreya C (2009) Gamma-phage lysin PlyG sequence-based synthetic peptides coupled with Qdot-nanocrystals are useful for developing detection methods for Bacillus anthracis by using its surrogates, B. anthracis-Sterne and B. cereus-4342. BMC Biotechnol 9:67PubMedCentralPubMedCrossRefGoogle Scholar
  53. 53.
    Savini V, Favaro M, Fontana C, Catavitello C, Balbinot A, Talia M, Febbo F, D’Antonio D (2009) Bacillus cereus heteroresistance to carbapenems in a cancer patient. J Hosp Infect 71:288–290PubMedCrossRefGoogle Scholar
  54. 54.
    Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler DR, Dean DH (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62:775–806PubMedCentralPubMedGoogle Scholar
  55. 55.
    Schofield DA, Westwater C (2009) Phage-mediated bioluminescent detection of Bacillus anthracis. J Appl Microbiol 107:1468–1478PubMedCrossRefGoogle Scholar
  56. 56.
    Schuch R, Nelson D, Fischetti VA (2002) A bacteriolytic agent that detects and kills Bacillus anthracis. Nature 418:884–889PubMedCrossRefGoogle Scholar
  57. 57.
    Schuch R, Fischetti VA (2006) Detailed genomic analysis of the Wbeta and gamma phages infecting Bacillus anthracis: implications for evolution of environmental fitness and antibiotic resistance. J Bacteriol 188:3037–3051PubMedCentralPubMedCrossRefGoogle Scholar
  58. 58.
    Schuch R, Pelzek AJ, Raz A, Euler CW, Ryan PA, Winer BY, Farnsworth A, Bhaskaran SS, Stebbins CE, Xu Y, Clifford A, Bearss DJ, Vankayalapati H, Goldberg AR, Fischetti VA (2013) Use of a bacteriophage lysin to identify a novel target for antimicrobial development. PLoS ONE 8:e60754PubMedCentralPubMedCrossRefGoogle Scholar
  59. 59.
    Smeesters PR, Dreze PA, Bousbata S, Parikka KJ, Timmery S, Hu X, Perez-Morga D, Deghorain M, Toussaint A, Mahillon J, Van Melderen L (2011) Characterization of a novel temperate phage originating from a cereulide-producing Bacillus cereus strain. Res Microbiol 162:446–459PubMedCrossRefGoogle Scholar
  60. 60.
    Son B, Yun J, Lim JA, Shin H, Heu S, Ryu S (2012) Characterization of LysB4, an endolysin from the Bacillus cereus-infecting bacteriophage B4. BMC Microbiol 12:33PubMedCentralPubMedCrossRefGoogle Scholar
  61. 61.
    Sozhamannan S, McKinstry M, Lentz SM, Jalasvuori M, McAfee F, Smith A, Dabbs J, Ackermann HW, Bamford JK, Mateczun A, Read TD (2008) Molecular characterization of a variant of Bacillus anthracis-specific phage AP50 with improved bacteriolytic activity. Appl Environ Microbiol 74:6792–6796PubMedCentralPubMedCrossRefGoogle Scholar
  62. 62.
    Stromsten NJ, Benson SD, Burnett RM, Bamford DH, Bamford JK (2003) The Bacillus thuringiensis linear double-stranded DNA phage Bam35, which is highly similar to the Bacillus cereus linear plasmid pBClin15, has a prophage state. J Bacteriol 185:6985–6989PubMedCentralPubMedCrossRefGoogle Scholar
  63. 63.
    Sulakvelidze A, Alavidze Z, Morris JG Jr (2001) Bacteriophage therapy. Antimicrob Agent Chemother 45:649–659CrossRefGoogle Scholar
  64. 64.
    Sullivan MJ, Petty NK, Beatson SA (2011) Easyfig: a genome comparison visualizer. Bioinformatics 27:1009–1010PubMedCentralPubMedCrossRefGoogle Scholar
  65. 65.
    Swanson MM, Reavy B, Makarova KS, Cock PJ, Hopkins DW, Torrance L, Koonin EV, Taliansky M (2012) Novel bacteriophages containing a genome of another bacteriophage within their genomes. PLoS ONE 7:e40683PubMedCentralPubMedCrossRefGoogle Scholar
  66. 66.
    Teeling H, Waldmann J, Lombardot T, Bauer M, Glockner FO (2004) TETRA: a web-service and a stand-alone program for the analysis and comparison of tetranucleotide usage patterns in DNA sequences. BMC Bioinf 5:163CrossRefGoogle Scholar
  67. 67.
    Thomas JA, Hardies SC, Rolando M, Hayes SJ, Lieman K, Carroll CA, Weintraub ST, Serwer P (2007) Complete genomic sequence and mass spectrometric analysis of highly diverse, atypical Bacillus thuringiensis phage 0305phi8-36. Virol 368:405–421CrossRefGoogle Scholar
  68. 68.
    Twort FW (1915) An investigation on the nature of ultra-microscopic viruses. Lancet 186:1241–1243CrossRefGoogle Scholar
  69. 69.
    Verheust C, Jensen G, Mahillon J (2003) pGIL01, a linear tectiviral plasmid prophage originating from Bacillus thuringiensis serovar israelensis. Microbiol 149:2083–2092CrossRefGoogle Scholar
  70. 70.
    Verheust C, Fornelos N, Mahillon J (2004) The Bacillus thuringiensis phage GIL01 encodes two enzymes with peptidoglycan hydrolase activity. FEMS Microbiol Lett 237:289–295PubMedGoogle Scholar
  71. 71.
    Verheust C, Fornelos N, Mahillon J (2005) GIL16, a new gram-positive tectiviral phage related to the Bacillus thuringiensis GIL01 and the Bacillus cereus pBClin15 elements. J Bacteriol 187:1966–1973PubMedCentralPubMedCrossRefGoogle Scholar
  72. 72.
    Vilas-Boas GT, Peruca AP, Arantes OM (2007) Biology and taxonomy of Bacillus cereus, Bacillus anthracis, and Bacillus thuringiensis. Can J Microbiol 53:673–687PubMedCrossRefGoogle Scholar
  73. 73.
    Volozhantsev NV, Oakley BB, Morales CA, Verevkin VV, Bannov VA, Krasilnikova VM, Popova AV, Zhilenkov EL, Garrish JK, Schegg KM, Woolsey R, Quilici DR, Line JE, Hiett KL, Siragusa GR, Svetoch EA, Seal BS (2012) Molecular characterization of podoviral bacteriophages virulent for Clostridium perfringens and their comparison with members of the Picovirinae. PloS ONE 7:e38283PubMedCentralPubMedCrossRefGoogle Scholar
  74. 74.
    Yuan Y, Gao M, Wu D, Liu P, Wu Y (2012) Genome characteristics of a novel phage from Bacillus thuringiensis showing high similarity with phage from Bacillus cereus. PLoS ONE 7:e37557PubMedCentralPubMedCrossRefGoogle Scholar
  75. 75.
    Yuan Y, Peng Q, Gao M (2012) Characteristics of a broad lytic spectrum endolysin from phage BtCS33 of Bacillus thuringiensis. BMC Microbiol 12:297PubMedCentralPubMedCrossRefGoogle Scholar
  76. 76.
    Zdobnov EM, Apweiler R (2001) InterProScan—an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847–848PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2013

Authors and Affiliations

  1. 1.Department of Food and Animal Biotechnology, Research Institute for Agriculture and Life Sciences, and Center for Food and BioconvergenceSeoul National UniversitySeoulKorea
  2. 2.Department of Agricultural Biotechnology, Research Institute for Agriculture and Life Sciences, and Center for Food and BioconvergenceSeoul National UniversitySeoulKorea
  3. 3.Department of Food Science and BiotechnologyKyung Hee UniversityYonginKorea

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