Genomic analysis of a phage and prophage from a strain Free

Abstract

Bacteriophages have been found to be the most abundant and also potentially most diverse biological entities on Earth. In the present study, phages were isolated rapidly and shown to have a high degree of diversity. The genomes of a newly isolated phage, phiCM3, and a prophage, proCM3, from the strain YM-03 were sequenced and characterized. Comparative genome analysis showed that the phiCM3 genome is highly similar to the genomes of eight other phages and seven of these phages were classified as the Wβ group of phages. Analysis of the differential evolution of the genes in the Wβ-group phages indicated that the genes encoding the antirepressor and tail fibre protein were more highly conserved than those encoding the major capsid protein, DNA replication protein, and RNA polymerase σ factor, which might have diverged to acquire mechanisms suitable for survival in different microbial hosts. Genome analysis of proCM3 revealed that proCM3 might be a defective phage because of mutations in the minor structural protein, and it was not inducible by mitomycin C treatment. The proCM3 genome was similar to those of two lytic phages in sequence, but had a different genomic structure, composed of three regions in a different order. These data suggest that the three phages might have had a common ancestor and that genome rearrangement might have occurred during evolution. The findings of this study enrich our current knowledge of phage diversity and evolution, especially for the Wβ-group and TP21-L-like phages, and may help the development of practical applications of phages.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.058735-0
2014-03-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/3/751.html?itemId=/content/journal/jgv/10.1099/vir.0.058735-0&mimeType=html&fmt=ahah

References

  1. Abshire T. G., Brown J. E., Ezzell J. W. 2005; Production and validation of the use of gamma phage for identification of Bacillus anthracis. . J Clin Microbiol 43:4780–4788 [View Article][PubMed]
    [Google Scholar]
  2. Ackermann H. W., Azizbekyan R. R., Emadi Konjin H. P., Lecadet M. M., Seldin L., Yu M. X. 1994; New Bacillus bacteriophage species. Arch Virol 135:333–344 [View Article][PubMed]
    [Google Scholar]
  3. Berngruber T. W., Weissing F. J., Gandon S. 2010; Inhibition of superinfection and the evolution of viral latency. J Virol 84:10200–10208 [View Article][PubMed]
    [Google Scholar]
  4. Bhattacharya D., Price D. C., Bicep C., Bapteste E., Sarwade M., Rajah V. D., Yoon H. S. 2013; Identification of a marine cyanophage in a protist single-cell metagenome assembly. J Phycol 49:207–212 [View Article]
    [Google Scholar]
  5. Biers E. J., Wang K., Pennington C., Belas R., Chen F., Moran M. A. 2008; Occurrence and expression of gene transfer agent genes in marine bacterioplankton. Appl Environ Microbiol 74:2933–2939 [View Article][PubMed]
    [Google Scholar]
  6. Bishop-Lilly K. A., Plaut R. D., Chen P. E., Akmal A., Willner K. M., Butani A., Dorsey S., Mokashi V., Mateczun A. J. other authors 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 9:246 [View Article][PubMed]
    [Google Scholar]
  7. Breitbart M., Rohwer F. 2005; Here a virus, there a virus, everywhere the same virus?. Trends Microbiol 13:278–284 [View Article][PubMed]
    [Google Scholar]
  8. Breitbart M., Salamon P., Andresen B., Mahaffy J. M., Segall A. M., Mead D., Azam F., Rohwer F. 2002; Genomic analysis of uncultured marine viral communities. Proc Natl Acad Sci U S A 99:14250–14255 [View Article][PubMed]
    [Google Scholar]
  9. Breitbart M., Hewson I., Felts B., Mahaffy J. M., Nulton J., Salamon P., Rohwer F. 2003; Metagenomic analyses of an uncultured viral community from human feces. J Bacteriol 185:6220–6223 [View Article][PubMed]
    [Google Scholar]
  10. Brüssow H., Canchaya C., Hardt W. D. 2004; Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560–602 [View Article][PubMed]
    [Google Scholar]
  11. Carey-Smith G. V., Billington C., Cornelius A. J., Hudson J. A., Heinemann J. A. 2006; Isolation and characterization of bacteriophages infecting Salmonella spp.. FEMS Microbiol Lett 258:182–186 [View Article][PubMed]
    [Google Scholar]
  12. Dai W., Hodes A., Hui W. H., Gingery M., Miller J. F., Zhou Z. H. 2010; Three-dimensional structure of tropism-switching Bordetella bacteriophage. Proc Natl Acad Sci U S A 107:4347–4352 [View Article][PubMed]
    [Google Scholar]
  13. Darling A. C. E., Mau B., Blattner F. R., Perna N. T. 2004; Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403 [View Article][PubMed]
    [Google Scholar]
  14. Dekel-Bird N. P., Avrani S., Sabehi G., Pekarsky I., Marston M. F., Kirzner S., Lindell D. 2013; Diversity and evolutionary relationships of T7-like podoviruses infecting marine cyanobacteria. Environ Microbiol 15:1476–1491 [View Article][PubMed]
    [Google Scholar]
  15. 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–e00012[PubMed] [CrossRef]
    [Google Scholar]
  16. Doulatov S., Hodes A., Dai L. X., Mandhana N., Liu M., Deora R., Simons R. W., Zimmerly S., Miller J. F. 2004; Tropism switching in Bordetella bacteriophage defines a family of diversity-generating retroelements. Nature 431:476–481 [View Article][PubMed]
    [Google Scholar]
  17. Edwards R. A., Rohwer F. 2005; Viral metagenomics. Nat Rev Microbiol 3:504–510 [View Article][PubMed]
    [Google Scholar]
  18. El-Arabi T. F., Griffiths M. W., She Y. M., Villegas A., Lingohr E. J., Kropinski A. M. 2013; Genome sequence and analysis of a broad-host range lytic bacteriophage that infects the Bacillus cereus group. Virol J 10:48 [View Article][PubMed]
    [Google Scholar]
  19. El Haddad L., Moineau S. 2013; Characterization of a Novel Panton-Valentine leukocidin (PVL)-encoding staphylococcal phage and its naturally PVL-lacking variant. Appl Environ Microbiol 79:2828–2832 [View Article][PubMed]
    [Google Scholar]
  20. Falkowski P. G., Fenchel T., Delong E. F. 2008; The microbial engines that drive Earth’s biogeochemical cycles. Science 320:1034–1039 [View Article][PubMed]
    [Google Scholar]
  21. Fischetti V. A. 2008; Bacteriophage lysins as effective antibacterials. Curr Opin Microbiol 11:393–400 [View Article][PubMed]
    [Google Scholar]
  22. Fogg P. C. M., Rigden D. J., Saunders J. R., McCarthy A. J., Allison H. E. 2011; Characterization of the relationship between integrase, excisionase and antirepressor activities associated with a superinfecting Shiga toxin encoding bacteriophage. Nucleic Acids Res 39:2116–2129 [View Article][PubMed]
    [Google Scholar]
  23. Fouts D. E., Rasko D. A., Cer R. Z., Jiang L. X., Fedorova N. B., Shvartsbeyn A., Vamathevan J. J., Tallon L., Althoff R. other authors 2006; Sequencing Bacillus anthracis typing phages gamma and cherry reveals a common ancestry. J Bacteriol 188:3402–3408 [View Article][PubMed]
    [Google Scholar]
  24. Gao M. Y., Li R. S., Dai S. Y., Wu Y., Yi D. 2008; Diversity of Bacillus thuringiensis strains from soil in China and their pesticidal activities. Biol Control 44:380–388 [View Article]
    [Google Scholar]
  25. García P., Martínez B., Obeso J. M., Lavigne R., Lurz R., Rodríguez A. 2009; Functional genomic analysis of two Staphylococcus aureus phages isolated from the dairy environment. Appl Environ Microbiol 75:7663–7673 [View Article][PubMed]
    [Google Scholar]
  26. Golais F., Hollý J., Vítkovská J. 2013; Coevolution of bacteria and their viruses. Folia Microbiol (Praha) 58:177–186 [View Article][PubMed]
    [Google Scholar]
  27. He J., Shao X. H., Zheng H. J., Li M. S., Wang J. P., Zhang Q. Y., Li L., Liu Z. D., Sun M. other authors 2010; Complete genome sequence of Bacillus thuringiensis mutant strain BMB171. J Bacteriol 192:4074–4075 [View Article][PubMed]
    [Google Scholar]
  28. Hendrix R. W., Smith M. C. M., Burns R. N., Ford M. E., Hatfull G. F. 1999; Evolutionary relationships among diverse bacteriophages and prophages: all the world’s a phage. Proc Natl Acad Sci U S A 96:2192–2197 [View Article][PubMed]
    [Google Scholar]
  29. Hobbie J. E., Daley R. J., Jasper S. 1977; Use of nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33:1225–1228[PubMed]
    [Google Scholar]
  30. Ioannou C., Schaeffer P. M., Dixon N. E., Soultanas P. 2006; Helicase binding to DnaI exposes a cryptic DNA-binding site during helicase loading in Bacillus subtilis. . Nucleic Acids Res 34:5247–5258 [View Article][PubMed]
    [Google Scholar]
  31. Ivanova N., Sorokin A., Anderson I., Galleron N., Candelon B., Kapatral V., Bhattacharyya A., Reznik G., Mikhailova N. other authors 2003; Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. . Nature 423:87–91 [View Article][PubMed]
    [Google Scholar]
  32. Jalasvuori M., Palmu S., Gillis A., Kokko H., Mahillon J., Bamford J. K. H., Fornelos N. 2013; Identification of five novel tectiviruses in Bacillus strains: analysis of a highly variable region generating genetic diversity. Res Microbiol 164:118–126 [View Article][PubMed]
    [Google Scholar]
  33. Jensen G. B., Hansen B. M., Eilenberg J., Mahillon J. 2003; The hidden lifestyles of Bacillus cereus and relatives. Environ Microbiol 5:631–640 [View Article][PubMed]
    [Google Scholar]
  34. Kaneko J., Kimura T., Narita S., Tomita T., Kamio Y. 1998; Complete nucleotide sequence and molecular characterization of the temperate staphylococcal bacteriophage phiPVL carrying Panton-Valentine leukocidin genes. Gene 215:57–67 [View Article][PubMed]
    [Google Scholar]
  35. Karlsson J. L., Cardoso-Palacios C., Nilsson A. S., Haggård-Ljungquist E. 2006; Evolution of immunity and host chromosome integration site of P2-like coliphages. J Bacteriol 188:3923–3935 [View Article][PubMed]
    [Google Scholar]
  36. Kikkawa H. S., 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 286:236–240 [View Article][PubMed]
    [Google Scholar]
  37. Klumpp J., Dorscht J., Lurz R., Bielmann R., Wieland M., Zimmer M., Calendar R., Loessner M. J. 2008; The terminally redundant, nonpermuted genome of Listeria bacteriophage A511: a model for the SPO1-like myoviruses of gram-positive bacteria. J Bacteriol 190:5753–5765 [View Article][PubMed]
    [Google Scholar]
  38. Klumpp J., Calendar R., Loessner M. J. 2010; Complete nucleotide sequence and molecular characterization of Bacillus phage TP21 and its relatedness to other phages with the same name. Viruses 2:961–971 [View Article][PubMed]
    [Google Scholar]
  39. Kwan T., Liu J., Dubow M., Gros P., Pelletier J. 2006; Comparative genomic analysis of 18 Pseudomonas aeruginosa bacteriophages. J Bacteriol 188:1184–1187 [View Article][PubMed]
    [Google Scholar]
  40. Labrie S. J., Frois-Moniz K., Osburne M. S., Kelly L., Roggensack S. E., Sullivan M. B., Gearin G., Zeng Q., Fitzgerald M. other authors 2013; Genomes of marine cyanopodoviruses reveal multiple origins of diversity. Environ Microbiol 15:1356–1376 [View Article][PubMed]
    [Google Scholar]
  41. Liao W., Song S. Y., Sun F., Jia Y. H., Zeng W. H., Pang Y. 2008; Isolation, characterization and genome sequencing of phage MZTP02 from Bacillus thuringiensis MZ1. Arch Virol 153:1855–1865 [View Article][PubMed]
    [Google Scholar]
  42. Loessner M. J., Maier S. K., 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 179:2845–2851[PubMed]
    [Google Scholar]
  43. Lucchini S., Desiere F., Brüssow H. 1999; Comparative genomics of Streptococcus thermophilus phage species supports a modular evolution theory. J Virol 73:8647–8656[PubMed]
    [Google Scholar]
  44. 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 354:1–15 [View Article][PubMed]
    [Google Scholar]
  45. 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 2012:543286[PubMed]
    [Google Scholar]
  46. Peng Q., Yuan Y., Gao M. 2013; Bacillus pumilus, a novel ginger rhizome rot pathogen in China. Plant Dis 97:1308–1315 [View Article]
    [Google Scholar]
  47. Porter C. J., Schuch R., Pelzek A. J., Buckle A. M., McGowan S., Wilce M. C. J., Rossjohn J., Russell R., Nelson D. other authors 2007; The 1.6 A crystal structure of the catalytic domain of PlyB, a bacteriophage lysin active against Bacillus anthracis. . J Mol Biol 366:540–550 [View Article][PubMed]
    [Google Scholar]
  48. Rohwer F. 2003; Global phage diversity. Cell 113:141 [View Article][PubMed]
    [Google Scholar]
  49. Rohwer F., Barott K. 2013; Viral information. Biol Philos 28:283–297 [View Article][PubMed]
    [Google Scholar]
  50. Schattner P., Brooks A. N., Lowe T. M. 2005; The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:Web Server issueW686–W689 [View Article][PubMed]
    [Google Scholar]
  51. Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., Zeigler D. R., Dean D. H. 1998; Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62:775–806[PubMed]
    [Google Scholar]
  52. Schuch R., Fischetti V. A. 2006; Detailed genomic analysis of the Wbeta and gamma phages infecting Bacillus anthracis: implications for evolution of environmental fitness and antibiotic resistance. J Bacteriol 188:3037–3051 [View Article][PubMed]
    [Google Scholar]
  53. Schuch R., Fischetti V. A. 2009; The secret life of the anthrax agent Bacillus anthracis: bacteriophage-mediated ecological adaptations. PLoS ONE 4:e6532 [View Article][PubMed]
    [Google Scholar]
  54. Schuch R., Nelson D., Fischetti V. A. 2002; A bacteriolytic agent that detects and kills Bacillus anthracis. . Nature 418:884–889 [View Article][PubMed]
    [Google Scholar]
  55. Sheehan M. M., Stanley E., Fitzgerald G. F., van Sinderen D. 1999; Identification and characterization of a lysis module present in a large proportion of bacteriophages infecting Streptococcus thermophilus. . Appl Environ Microbiol 65:569–577[PubMed]
    [Google Scholar]
  56. Susskind M. M., Botstein D. 1975; Mechanism of action of Salmonella phage P22 antirepressor. J Mol Biol 98:413–424 [View Article][PubMed]
    [Google Scholar]
  57. Swanson M. M., Reavy B., Makarova K. S., Cock P. J., Hopkins D. W., Torrance L., Koonin E. V., Taliansky M. 2012; Novel bacteriophages containing a genome of another bacteriophage within their genomes. PLoS ONE 7:e40683 [View Article][PubMed]
    [Google Scholar]
  58. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega 5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  59. Thomas J. A., Hardies S. C., Rolando M., Hayes S. J., Lieman K., Carroll C. A., Weintraub S. T., Serwer P. 2007; Complete genomic sequence and mass spectrometric analysis of highly diverse, atypical Bacillus thuringiensis phage 0305phi8-36. Virology 368:405–421 [View Article][PubMed]
    [Google Scholar]
  60. Vale P. F., Choisy M., Froissart R., Sanjuán R., Gandon S. 2012; The distribution of mutational fitness effects of phage φX174 on different hosts. Evolution 66:3495–3507 [View Article][PubMed]
    [Google Scholar]
  61. Vilas-Bôas G. T., Peruca A. P. S., Arantes O. M. N. 2007; Biology and taxonomy of Bacillus cereus, Bacillus anthracis, and Bacillus thuringiensis. . Can J Microbiol 53:673–687 [View Article][PubMed]
    [Google Scholar]
  62. Wang S., Kong J., Zhang X. 2008; Identification and characterization of the two-component cell lysis cassette encoded by temperate bacteriophage phiPYB5 of Lactobacillus fermentum. . J Appl Microbiol 105:1939–1944 [View Article][PubMed]
    [Google Scholar]
  63. Weinbauer M. G. 2004; Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181 [View Article][PubMed]
    [Google Scholar]
  64. Weitz J. S., Poisot T., Meyer J. R., Flores C. O., Valverde S., Sullivan M. B., Hochberg M. E. 2013; Phage-bacteria infection networks. Trends Microbiol 21:82–91 [View Article][PubMed]
    [Google Scholar]
  65. Yang W., Steitz T. A. 1995; Crystal structure of the site-specific recombinase gamma delta resolvase complexed with a 34 bp cleavage site. Cell 82:193–207 [View Article][PubMed]
    [Google Scholar]
  66. Young I., Wang I. N., Roof W. D. 2000; Phages will out: strategies of host cell lysis. Trends Microbiol 8:120–128 [View Article][PubMed]
    [Google Scholar]
  67. Yuan Y. H., Peng Q., Gao M. Y. 2012a; Characteristics of a broad lytic spectrum endolysin from phage BtCS33 of Bacillus thuringiensis. . BMC Microbiol 12:297 [View Article][PubMed]
    [Google Scholar]
  68. Yuan Y. H., Gao M. Y., Wu D. D., Liu P. M., Wu Y. 2012b; Genome characteristics of a novel phage from Bacillus thuringiensis showing high similarity with phage from Bacillus cereus. . PLoS ONE 7:e37557 [View Article][PubMed]
    [Google Scholar]
  69. Zafar N., Mazumder R., Seto D. 2002; CoreGenes: a computational tool for identifying and cataloging “core” genes in a set of small genomes. BMC Bioinformatics 3:12 [View Article][PubMed]
    [Google Scholar]
  70. Zecchi L., Lo Piano A., Suzuki Y., Cañas C., Takeyasu K., Ayora S. 2012; Characterization of the Holliday junction resolving enzyme encoded by the Bacillus subtilis bacteriophage SPP1. PLoS ONE 7:e48440 [View Article][PubMed]
    [Google Scholar]
  71. Zhang W. K., Allen S., Roberts C. J., Soultanas P. 2006; The Bacillus subtilis primosomal protein DnaD untwists supercoiled DNA. J Bacteriol 188:5487–5493 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.058735-0
Loading
/content/journal/jgv/10.1099/vir.0.058735-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed