Skip to main content
Log in

Identification and characterization of a novel Geobacillus thermoglucosidasius bacteriophage, GVE3

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

The study of extremophilic phages may reveal new phage families as well as different mechanisms of infection, propagation and lysis to those found in phages from temperate environments. We describe a novel siphovirus, GVE3, which infects the thermophile Geobacillus thermoglucosidasius. The genome size is 141,298 bp (G+C 29.6 %), making it the largest Geobacillus spp-infecting phage known. GVE3 appears to be most closely related to the recently described Bacillus anthracis phage vB_BanS_Tsamsa, rather than Geobacillus-infecting phages described thus far. Tetranucleotide usage deviation analysis supports this relationship, showing that the GVE3 genome sequence correlates best with B. anthracis and Bacillus cereus genome sequences, rather than Geobacillus spp genome sequences.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Ackermann HW (2007) 5500 Phages examined in the electron microscope. Arch Virol 152:227–243

    Article  CAS  PubMed  Google Scholar 

  2. Ackermann HW, Heldal M (2010) Basic electron microscopy of aquatic viruses. In: Manual of aquatic viral ecology, Chapter 18. American Society of Limnology and Oceanography, Inc., p 182–192

  3. Adriaenssens EM, van Zyl LJ, de Maayer P, Rubagotti E, Rybicki E, Tuffin M, Cowan DA (2014) Metagenomic analysis of the viral community in Namib Desert hypoliths. Environ Microbiol. doi:10.1111/1462-2920.12528

    PubMed  Google Scholar 

  4. Ahn D-G, Kim S-I, Rhee J-K, Kim KP, Pan J-G, Oh J-W (2006) TTSV1, a new virus-like particle isolated from the hyperthermophilic crenarchaeote Thermoproteus tenax. Virol 351:280–290

    Article  CAS  Google Scholar 

  5. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  6. Arnold HP, Zillig W, Ziese U, Holz I, Crosby M, Utterback T, Weidmann JF, Kristjanson JK, Klenk HP, Nelson KE, Fraser CM (2000) A novel lipothrixvirus, SIFV, of the extremely thermophilic crenarchaeon Sulfolobus. Virol 267:252–266

    Article  CAS  Google Scholar 

  7. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: Rapid annotations using subsystems technology. BMC Genomics 9:75

    Article  PubMed Central  PubMed  Google Scholar 

  8. Belcaid M, Bergeron A, Poisson G (2011) The evolution of the tape measure protein: units, duplications and losses. BMC Bioinform 12:S10

    Article  CAS  Google Scholar 

  9. Betley JN, Frith MC, Graber JH, Choo S, Deshler JO (2002) A ubiquitous and conserved signal for RNA localization in chordates. Curr Biol 12:1756–1761

    Article  CAS  PubMed  Google Scholar 

  10. Blatny JM, Godager L, Lunde M, Nes IF (2004) Complete genome sequence of the Lactococcus lactis temperate phage φLC3: comparative analysis of φLC3 and its relatives in lactococci and streptococci. Virology 318:231–244

    Article  CAS  PubMed  Google Scholar 

  11. Bodnarz JW, Zempsky W, Warder D, Bergson C, Ward DC (1983) Effect of nucleotide analogs on the cleavage of DNA by the restriction enzymes AluI, DdeI, HinfI, RsaI, and TaqI. J Biol Chem 258:15206–15213

    Google Scholar 

  12. Bohlin J, van Passel MWJ, Snipen L, Kristoffersen AB, Ussery D, Hardy SP (2012) Relative entropy differences in bacterial chromosomes, plasmids, phages and genomic islands. BMC Genomics 13:66–78

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Bryan MJ, Burroughs NJ, Spence EM, Clokie MRJ, Mann NH, Bryan SJ (2008) Evidence for the intense exchange of MazG in marine cyanophages by horizontal gene transfer. PLOS One. doi:10.1371/journal.pone.0002048

    Google Scholar 

  14. Bullard JM, Williams JC, Acker WK, Jacobi C, Janjic N, McHenry CS (2002) DNA polymerase III holoenzyme from Thermus thermophiles identification, expression, purification of components, and use to reconstitute a processive replicase. J Biol Chem 277:13401–13408

    Article  CAS  PubMed  Google Scholar 

  15. Burgess SA, Lindsay D, Flint SH (2010) Thermophilic bacilli and their importance in dairy processing. Int J Food Microbiol 144:215–225

    Article  CAS  PubMed  Google Scholar 

  16. Buxton RS, Hammer-Jespersen K, Hansen TD (1978) Insertion of bacteriophage lambda into the deo operon of Escherichia coli K-12 and isolation of plaque-forming λdeo + transducing bacteriophages. J Bacteriol 136:668–681

    PubMed Central  CAS  PubMed  Google Scholar 

  17. Chen Y, Wei D, Wang Y, Zhang X (2013) The role of interactions between bacterial chaperone, aspartate aminotransferase, and viral protein during virus infection in high temperature environment: the interactions between bacterium and virus proteins. BMC Microbiol 13:48

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Clokie MRJ, Millard AD, Letarov AV, Heaphy S (2011) Phages in nature. Bacteriophage 1:31–45

    Article  PubMed Central  PubMed  Google Scholar 

  19. Cripps RE, Eley K, Leak DJ, Rudd B, Taylor M, Todd M, Boakes S, Martin S, Atkinson T (2009) Metabolic engineering of Geobacillus thermoglucosidasius for high yield ethanol production. Metab Eng 11:398–408

    Article  CAS  PubMed  Google Scholar 

  20. Doi K, Mori K, Martono H, Nagayoshi Y, Fujino Y, Tashiro K, Kuhara S, Ohshima T (2013) Draft Genome Sequence of Geobacillus kaustophilus GBlys, a Lysogenic Strain with Bacteriophage OH2. Genome Announc 1:e00634–e00713

    PubMed Central  PubMed  Google Scholar 

  21. Dwivedi B, Xue B, Lundin D, Edwards RA, Breitbart M (2013) A bioinformatic analysis of ribonucleotide reductase genes in phage genomes and metagenomes. BMC Evol Biol 13:33

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Edgar R, Qimron U (2010) The Escherichia coli CRISPR system protects from lysogenization, lysogens, and prophage induction. J Bacteriol 192:6291–6294

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Feiss M, Siegele DA (1979) Packaging of the bacteriophage lambda chromosome: dependence of cos cleavage on chromosome length. Virology 92:190–200

    Article  CAS  PubMed  Google Scholar 

  24. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  25. Ganz HH, Law C, Schmuki M, Eichenseher F, Calendar R, Loessner MJ, Getz WM, Korlach J, Beyer W, Klumpp J (2014) Novel giant Siphovirus from Bacillus anthracis features unusual genome characteristics. PLoS One 9:e85972

    Article  PubMed Central  PubMed  Google Scholar 

  26. Goldsmith DB, Crosti G, Dwivedi B, McDaniel LD, Varsani A, Suttle CA, Weinbauer MG, Sandaa RA, Breitbart M (2011) Development of phoH as a novel signature gene for assessing marine phage diversity. Appl Environ Microbiol 77:7730–7739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Gross M, Marianovsky I, Glaser G (2006) MazG—a regulator of programmed cell death in Escherichia coli. Mol Microbiol 59:590–601

    Article  CAS  PubMed  Google Scholar 

  28. Hargreaves KR, Kropinski AM, Clokie MRJ (2014) Bacteriophage behavioral ecology: how phages alter their bacterial host’s habits. Bacteriophage. doi:10.4161/bact.29866

    PubMed Central  PubMed  Google Scholar 

  29. Heler R, Marraffini LA, Bikard D (2014) Adapting to new threats: the generation of memory by CRISPR-Cas immune systems. Mol Microbiol. doi:10.1111/mmi.12640

    PubMed Central  PubMed  Google Scholar 

  30. Höök-Nikanne J, Berg DE, Peek RM Jr, Kersulyte D, Tummuru MKR, Blaser MJ (1999) DNA sequence conservation and diversity in transposable element IS605 of Helicobacter pylori. Helicobacter 3:79–85

    Article  Google Scholar 

  31. Iyer LM, Koonin EV, Aravind L (2002) Extensive domain shuffling in transcription regulators of DNA viruses and implications for the origin of fungal APSES transcription factors. Gen. Biol 3:research0012.1–research0012.11

    Article  Google Scholar 

  32. Jin M, Ye T, Zhang X (2013) Roles of bacteriophage GVE2 endolysin in host lysis at high temperatures. Microbiology 159:1597–1605

    Article  CAS  PubMed  Google Scholar 

  33. Jin M, Chen Y, Xu C, Zhang X (2014) The effect of inhibition of host MreB on the infection of thermophilic phage GVE2 in high temperature environment. Sci Rep 4:4823

    PubMed Central  PubMed  Google Scholar 

  34. Kotze AA, Tuffin IM, Deane SM, Rawlings DE (2006) Cloning and characterization of the chromosomal arsenic resistance genes from Acidithiobacillus caldus and enhanced arsenic resistance on conjugal transfer of ars genes located on transposon TnAtcArs. Microbiology 152:3551–3560

    Article  CAS  PubMed  Google Scholar 

  35. Krogh S, Jørgensen ST, Devine KM (1998) Lysis genes of the Bacillus subtilis defective prophage PBSX. J Bacteriol 180:2110–2117

    PubMed Central  CAS  PubMed  Google Scholar 

  36. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580

    Article  CAS  PubMed  Google Scholar 

  37. Kumaran D, Eswaramoorthy S, Studier FW, Swaminathan S (2005) Structure and mechanism of ADP-ribose-1-monophosphatase (Appr-1-pase), a ubiquitous cellular processing enzyme. Prot Sci 14:719–726

    Article  CAS  Google Scholar 

  38. Lang BF, Laforest MJ, Burger G (2007) Mitochondrial introns: a critical view. Trends Genet 23:119–125

    Article  CAS  PubMed  Google Scholar 

  39. Laslett D, Canback B (2004) ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucl Acids Res 32:11–16

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Le Romancer M, Gaillard M, Geslin C, Prieur D (2007) Viruses in extreme environments. In: Amils Ricardo, Ellis-Evans Cynan, Hinghofer-Szalkay Helmut (eds) Life in extreme environments. Springer, Netherlands, pp 99–113

    Google Scholar 

  41. Levine M, Truesdall S, Ramakrishan T, Bronson MJ (1975) Dual control of lysogeny by bacteriophage P22: an antirepressor locus and its controlling elements. J Mol Biol 91:421–438

    Article  CAS  PubMed  Google Scholar 

  42. Lin PP, Rabe KS, Takasumi JL, Kadisch M, Arnold FH, Liao JC (2014) Isobutanol production at elevated temperatures in thermophilic Geobacillus thermoglucosidasius. Metab Eng 24:1–8

    Article  CAS  PubMed  Google Scholar 

  43. Liu B, Wu S, Song Q, Zhang X, Xie L (2006) Two novel bacteriophages of thermophilic bacteria isolated from Deep-Sea hydrothermal fields. Curr Microbiol 53:163–166

    Article  CAS  PubMed  Google Scholar 

  44. Liu B, Zhang X (2008) Deep-sea thermophilic Geobacillus bacteriophage GVE2 transcriptional profile and proteomic characterization of virions. Appl Microbiol Biotechnol 80:697–707

    Article  CAS  PubMed  Google Scholar 

  45. Liu B, Zhou F, Wu S, Xu Y, Zhang X (2009) Genomic and proteomic characterization of a thermophilic Geobacillus bacteriophage GBSV1. Res Microbiol 160:166–170

    Article  CAS  PubMed  Google Scholar 

  46. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucl Acids Res 25:955–964

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Magnusson LU, Farewell A, Nystrom T (2005) ppGpp: a global regulator in Escherichia coli. Trends Microbiol 13:236–242

    Article  CAS  PubMed  Google Scholar 

  48. Marraffini LA, Sontheimer EJ (2010) CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 11:181–190

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Marians KJ, Hiasa H, Kim DR, McHenry C (1998) Role of the core DNA polymerase III subunits at the replication fork: ALPHA is the only subunit required for processive replication. J Biol Chem 273:2452–2457

    Article  CAS  PubMed  Google Scholar 

  50. Marks TJ, Hamilton PT (2014) Characterization of a thermophilic bacteriophage of Geobacillus kaustophilus. Arch Virol 159:2771–2775

    Article  CAS  PubMed  Google Scholar 

  51. McClelland M, Nelson M, Raschke E (1994) Effect of site-specific modification on restriction endonucleases and DNA modification methyltransferases. Nucl Acids Res 22:3640–3659

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  52. Millen AM, Horvath P, Boyaval P, Romero DA (2012) Mobile CRISPR/Cas-mediated bacteriophage resistance in Lactococcus lactis. PLoS One 7:e51663

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  53. Moser MJ, DiFrancesco RA, Gowda K, Klingele AJ, Sugar DR, Stocki S, Mead DA, Schoenfeld TW (2012) Thermostable DNA polymerase from a viral metagenome is a potent RT-PCR enzyme. PLOS One. doi:10.1371/journal.pone.0038371

    Google Scholar 

  54. Nazina TN, Tourova TP, Poltaraus AB, Novikova EV, Grigoryan AA, Ivanova AE, Lysenko AM, Petrunyaka VV, Osipov GA, Belyaev SS, Ivanov MV (2001) Taxonomic study of aerobic thermophilic bacilli: descriptions of Geobacillus subterraneus gen. nov., sp. nov. and Geobacillus uzenensis sp. nov. from petroleum reservoirs and transfer of Bacillus stearothermophilus, Bacillus thermocatenulatus, Bacillus thermoleovorans, Bacillus kaustophilus, Bacillus thermoglucosidasius and Bacillus thermodenitrificans to Geobacillus as the new combinations G. stearothermophilus, G. thermocatenulatus, G. thermoleovorans, G. kaustophilus, G. thermoglucosidasius and G. thermodenitrificans. IJSEM 51:433–446

    CAS  PubMed  Google Scholar 

  55. Neubort S, Marmur J (1973) Synthesis of the unusual DNA of Bacillus subtilis bacteriophage SP-15. J Virol 12:1078–1084

    PubMed Central  CAS  PubMed  Google Scholar 

  56. Østergaard S, Brøndsted L, Vogensen FK (2001) Identification of a replication protein and repeats essential for DNA replication of the temperate lactococcal bacteriophage TP901-1. Appl Environ Microbiol 67:774–781

    Article  PubMed Central  PubMed  Google Scholar 

  57. Payeta JP, Suttle CA (2013) To kill or not to kill: The balance between lytic and lysogenic viral infection is driven by trophic status. Limnol Oceanogr 58:465–474

    Google Scholar 

  58. Peduzzi P, Gruber M, Gruber M, Schager M (2014) The virus’s tooth: cyanophages affect an African flamingo population in a bottom-up cascade. ISME J 8:1346–1351

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  59. Plotka M, Kaczorowska A-K, Stefanska A, Morzywolek A, Fridjonsson OH, Dunin-Horkawicz S, Kozlowski L, Hreggvidsson GO, Kristjansson JK, Dabrowski S, Bujnicki JM, Kaczorowskia T (2013) Novel highly thermostable endolysin from Thermus scotoductus MAT2119 bacteriophage Ph2119 with amino acid sequence similarity to Eukaryotic peptidoglycan recognition proteins. Appl Environ Microbiol 80:886–895

    Article  PubMed  Google Scholar 

  60. Pride DT, Wassenaar TM, Ghose C, Blaser MJ (2006) Evidence of host-virus co-evolution in tetranucleotide usage patterns of bacteriophages and eukaryotic viruses. BMC Genomics. doi:10.1186/1471-2164-7-8

    PubMed Central  PubMed  Google Scholar 

  61. Quiles-Puchalt N, Tormo-Más MA, Campoy S, Toledo-Arana A, Monedero V, Lasa I, Novick RP, Christie GE, Penadés JR (2013) A super-family of transcriptional activators regulates bacteriophage packaging and lysis in Gram-positive bacteria. Nucl Acids Res 41:7260–7275

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  62. Rice G, Stedman K, Snyder J, Wiedenheft B, Willits D, Brumfield S, McDermott T, Young MJ (2001) Viruses from extreme thermal environments. Proc Nat Acad Sci 98:13341–13345

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  63. Riipinen KA, Alatossava T (2004) Two self-splicing group I introns interrupt two late transcribed genes of prolate-headed Lactobacillus delbrueckii phage JCL1032. Arch Virol 149:2013–2024

    CAS  PubMed  Google Scholar 

  64. Rocha EPC, Danchin A (2002) Base composition bias might result from competition for metabolic resources. Trends Genet 18:291–294

    Article  CAS  PubMed  Google Scholar 

  65. Sakaguchi Y, Hayashi T, Kurokawa K, Nakayama K, Oshima K, Fujinaga Y, Ohnishi M, Ohtsubo E, Hattori M, Oguma K (2005) The genome sequence of Clostridium botulinum type C neurotoxin-converting phage and the molecular mechanisms of unstable lysogeny. Proc Nat Acad Sci 102:17472–17477

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  66. Savalia D, Westblade LF, Goel M, Florens L, Kemp P, Akulenko N, Pavlova O, Padovan JC, Chait BT, Washburn MP, Ackermann HW, Mushegian A, Gabisonia T, Molineux I, Severinov K (2008) Genomic and proteomic analysis of phiEco32, a novel Escherichia coli phage. J Mol Biol 377:774–789

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  67. Schmidt TR, Scott EJ II, Dyer DW (2011) Whole-genome phylogenies of the family Bacillaceae and expansion of the sigma factor gene family in the Bacillus cereus species-group. BMC Genomics 12:430

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  68. Schoenfeld T, Patterson M, Richardson PM, Wommack KE, Young M, Mead D (2008) Assembly of viral metagenomes from yellowstone hot springs. Appl Environ Microbiol 74:4164–4174

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  69. Seco E, Zinder J, Manhart CM, Piano AL, McHenry C, Ayora S (2013) Bacteriophage SPP1 in vitro DNA replication strategies promote viral and disable host replication. Nucl Acid Res 41:1711–1721

    Article  CAS  Google Scholar 

  70. Sevostyanova A, Djordjevic M, Kuznedelov K, Naryshkina T, Gelfand MS, Severinov K, Minakhin L (2007) Temporal regulation of viral transcription during development of Thermus thermophilus bacteriophage ϕYS40. J Mol Biol 366:420–435

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  71. Sime-Ngando ST, Lucas S, Robin A, Tucker KP, Colombet J, Bettarel Y, Desmond E, Gribaldo S, Forterre P, Breitbart M, Prangishvili D (2010) Diversity of virus–host systems in hypersaline Lake Retba. Environ Microbiol 8:1956–1972

    Google Scholar 

  72. Song Q, Zhang X (2008) Characterization of a novel non-specific nuclease from thermophilic bacteriophage GBSV1. BMC Biotechnol 8:43

    Article  PubMed Central  PubMed  Google Scholar 

  73. Song Q, Ye T, Zhang X (2011) Proteins responsible for lysogeny of deep-sea thermophilic bacteriophage GVE2 at high temperature. Gene 479:1–9

    Article  CAS  PubMed  Google Scholar 

  74. Sorokin DY, Berben T, Melton ED, Overmars L, Vavourakis CD, Muyzer G (2014) Microbial diversity and biogeochemical cycling in soda lakes. Extremophiles 18:791–809

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  75. Sternberg N, Coulby J (1990) Cleavage of the bacteriophage P1 packaging site (pac) is regulated by adenine methylation. Proc Natl Acad. Sci 87:8070–8074

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  76. Suttle CA (2005) Viruses in the sea. Nature 437:356–361

    Article  CAS  PubMed  Google Scholar 

  77. Suzuki H, Yoshida K (2012) Genetic transformation of Geobacillus kaustophilus HTA426 by conjugative transfer of host-mimicking plasmids. J Microbiol Biotechnol 22:1279–1287

    Article  CAS  PubMed  Google Scholar 

  78. Szekera K, Zhou X, Schwab T, Casanueva A, Cowan D, Mikhailopulo IA, Neubauer P (2012) Comparative investigations on thermostable pyrimidine nucleoside phosphorylases from Geobacillus thermoglucosidasius and Thermus thermophiles. J Mol Cat B Enzymatic 84:27–34

    Article  Google Scholar 

  79. Taylor MP, Eley KL, Martin S, Tuffin MI, Burton SG, Cowan DA (2009) Thermophilic ethanologenesis: future prospects for second-generation bioethanol production. Trends Biotechnol 27:398–405

    Article  CAS  PubMed  Google Scholar 

  80. Torrents E (2014) Ribonucleotide reductases: essential enzymes for bacterial life. Front Cell Infect Microbiol. doi:10.3389/fcimb.2014.00052

    PubMed Central  PubMed  Google Scholar 

  81. Viedma PM, Abriouel H, Omar NB, Lopez RL, Valdivia E, Gálvez A (2009) Inactivation of Geobacillus stearothermophilus in canned food and coconut milk samples by addition of enterocin AS-48. Food Microbiol 26:289–293

    Article  CAS  PubMed  Google Scholar 

  82. Wang Y, Zhang X (2008) Identification and characterization of a novel thymidylate synthase from deep-sea thermophilic bacteriophage Geobacillus virus E2. Virus Genes 37:218–224

    Article  PubMed  Google Scholar 

  83. Wang Y, Zhang X (2010) Genome analysis of deep-sea thermophilic phage D6E. Appl Environ Microbiol 76:7861–7866

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  84. Wei D, Zhang X (2010) Proteomic analysis of interactions between a deep-sea thermophilic bacteriophage and its host at high temperature. J Virol 84:2365–2373

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  85. Weinberger AD, Sun CL, Plucinski MM, Denef VJ, Thomas BC, Horvath P, Barrangou R, Gilmore MS, Getz WM, Banfield JF (2012) Persisting viral sequences shape microbial CRISPR based immunity. PLoS One 8:e1002475

    CAS  Google Scholar 

  86. Westra ER, Swarts DC, Staals RHJ, Jore MM, Brouns SJJ, van der Oost J (2012) The CRISPRs, they are A-Changin’: How prokaryotes generate adaptive immunity. Annual Rev Genet 46:311–339

    Article  CAS  Google Scholar 

  87. Zhou Y, Liang Y, Lynch K, Dennis JJ, Wishart DS (2011) PHAST: a fast phage search tool. Nucl Acids Res 39:347–352

    Article  Google Scholar 

  88. Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. Edited in Evolving Genes and Proteins by Bryson V and Vogel HJ (eds). Academic Press, New York, pp. 97–166

Download references

Acknowledgments

The authors wish to thank TMO Renewables for the gift of the GVE3 phage. This work was funded by the National Research Foundation (NRF) of South Africa. The authors declare no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leonardo Joaquim van Zyl.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 731 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

van Zyl, L.J., Sunda, F., Taylor, M.P. et al. Identification and characterization of a novel Geobacillus thermoglucosidasius bacteriophage, GVE3. Arch Virol 160, 2269–2282 (2015). https://doi.org/10.1007/s00705-015-2497-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-015-2497-9

Keywords

Navigation