1887

Abstract

Mycobacteriophages BPs, Angel and Halo are closely related viruses isolated from , and possess the smallest known mycobacteriophage genomes, 41 901 bp, 42 289 bp and 41 441 bp, respectively. Comparative genome analysis reveals a novel class of ultra-small mobile genetic elements; BPs and Halo each contain an insertion of the proposed mobile elements MPME1 and MPME2, respectively, at different locations, while Angel contains neither. The close similarity of the genomes provides a comparison of the pre- and post-integration sequences, revealing an unusual 6 bp insertion at one end of the element and no target duplication. Nine additional copies of these mobile elements are identified in a variety of different contexts in other mycobacteriophage genomes. In addition, BPs, Angel and Halo have an unusual lysogeny module in which the repressor and integrase genes are closely linked. The site is located within the repressor-coding region, such that prophage formation results in expression of a C-terminally truncated, but active, form of the repressor.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.030486-0
2009-09-01
2019-10-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/9/2962.html?itemId=/content/journal/micro/10.1099/mic.0.030486-0&mimeType=html&fmt=ahah

References

  1. Bardarov, S., Kriakov, J., Carriere, C., Yu, S., Vaamonde, C., McAdam, R. A., Bloom, B. R., Hatfull, G. F. & Jacobs, W. R., Jr ( 1997; ). Conditionally replicating mycobacteriophages: a system for transposon delivery to Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 94, 10961–10966.[CrossRef]
    [Google Scholar]
  2. Bardarov, S., Bardarov, S., Jr, Pavelka, M. S., Jr, Sambandamurthy, V., Larsen, M., Tufariello, J., Chan, J., Hatfull, G. & Jacobs, W. R., Jr ( 2002; ). Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology 148, 3007–3017.
    [Google Scholar]
  3. Brown, K. L., Sarkis, G. J., Wadsworth, C. & Hatfull, G. F. ( 1997; ). Transcriptional silencing by the mycobacteriophage L5 repressor. EMBO J 16, 5914–5921.[CrossRef]
    [Google Scholar]
  4. Brussow, H. ( 2001; ). Phages of dairy bacteria. Annu Rev Microbiol 55, 283–303.[CrossRef]
    [Google Scholar]
  5. Donnelly-Wu, M. K., Jacobs, W. R., Jr & Hatfull, G. F. ( 1993; ). Superinfection immunity of mycobacteriophage L5: applications for genetic transformation of mycobacteria. Mol Microbiol 7, 407–417.[CrossRef]
    [Google Scholar]
  6. Ford, M. E., Sarkis, G. J., Belanger, A. E., Hendrix, R. W. & Hatfull, G. F. ( 1998a; ). Genome structure of mycobacteriophage D29: implications for phage evolution. J Mol Biol 279, 143–164.[CrossRef]
    [Google Scholar]
  7. Ford, M. E., Stenstrom, C., Hendrix, R. W. & Hatfull, G. F. ( 1998b; ). Mycobacteriophage TM4: genome structure and gene expression. Tuber Lung Dis 79, 63–73.[CrossRef]
    [Google Scholar]
  8. Freitas-Vieira, A., Anes, E. & Moniz-Pereira, J. ( 1998; ). The site-specific recombination locus of mycobacteriophage Ms6 determines DNA integration at the tRNAAla gene of Mycobacterium spp. Microbiology 144, 3397–3406.[CrossRef]
    [Google Scholar]
  9. Fullner, K. J. & Hatfull, G. F. ( 1997; ). Mycobacteriophage L5 infection of Mycobacterium bovis BCG: implications for phage genetics in the slow-growing mycobacteria. Mol Microbiol 26, 755–766.[CrossRef]
    [Google Scholar]
  10. Guynet, C., Hickman, A. B., Barabas, O., Dyda, F., Chandler, M. & Ton-Hoang, B. ( 2008; ). In vitro reconstitution of a single-stranded transposition mechanism of IS608. Mol Cell 29, 302–312.[CrossRef]
    [Google Scholar]
  11. Hatfull, G. F. ( 2000; ). Molecular genetics of mycobacteriophages. In Molecular Genetics of the Mycobacteria, pp. 37–54. Edited by G. F. Hatfull & W. R. Jacobs, Jr. Washington, DC: American Society for Microbiology.
  12. Hatfull, G. F. ( 2006; ). Mycobacteriophages. In The Bacteriophages, pp. 602–620. Edited by R. Calendar. New York: Oxford University Press.
  13. Hatfull, G. F. & Sarkis, G. J. ( 1993; ). DNA sequence, structure and gene expression of mycobacteriophage L5: a phage system for mycobacterial genetics. Mol Microbiol 7, 395–405.[CrossRef]
    [Google Scholar]
  14. Hatfull, G. F., Pedulla, M. L., Jacobs-Sera, D., Cichon, P. M., Foley, A., Ford, M. E., Gonda, R. M., Houtz, J. M., Hryckowian, A. J. & other authors ( 2006; ). Exploring the mycobacteriophage metaproteome: phage genomics as an educational platform. PLoS Genet 2, e92 [CrossRef]
    [Google Scholar]
  15. Hatfull, G. F., Cresawn, S. G. & Hendrix, R. W. ( 2008; ). Comparative genomics of the mycobacteriophages: insights into bacteriophage evolution. Res Microbiol 159, 332–339.[CrossRef]
    [Google Scholar]
  16. Hendrix, R. W. ( 2002; ). Bacteriophages: evolution of the majority. Theor Popul Biol 61, 471–480.[CrossRef]
    [Google Scholar]
  17. Jacobs, W. R., Jr, Tuckman, M. & Bloom, B. R. ( 1987; ). Introduction of foreign DNA into mycobacteria using a shuttle phasmid. Nature 327, 532–535.[CrossRef]
    [Google Scholar]
  18. Jacobs, W. R., Jr, Barletta, R. G., Udani, R., Chan, J., Kalkut, G., Sosne, G., Kieser, T., Sarkis, G. J., Hatfull, G. F. & Bloom, B. R. ( 1993; ). Rapid assessment of drug susceptibilities of Mycobacterium tuberculosis by means of luciferase reporter phages. Science 260, 819–822.[CrossRef]
    [Google Scholar]
  19. Jain, S. & Hatfull, G. F. ( 2000; ). Transcriptional regulation and immunity in mycobacteriophage Bxb1. Mol Microbiol 38, 971–985.
    [Google Scholar]
  20. Katsura, I. ( 1987; ). Determination of bacteriophage lambda tail length by a protein ruler. Nature 327, 73–75.[CrossRef]
    [Google Scholar]
  21. Katsura, I. & Hendrix, R. W. ( 1984; ). Length determination in bacteriophage lambda tails. Cell 39, 691–698.[CrossRef]
    [Google Scholar]
  22. Kersulyte, D., Velapatino, B., Dailide, G., Mukhopadhyay, A. K., Ito, Y., Cahuayme, L., Parkinson, A. J., Gilman, R. H. & Berg, D. E. ( 2002; ). Transposable element ISHp608 of Helicobacter pylori: nonrandom geographic distribution, functional organization, and insertion specificity. J Bacteriol 184, 992–1002.[CrossRef]
    [Google Scholar]
  23. Kim, A. I., Ghosh, P., Aaron, M. A., Bibb, L. A., Jain, S. & Hatfull, G. F. ( 2003; ). Mycobacteriophage Bxb1 integrates into the Mycobacterium smegmatis groEL1 gene. Mol Microbiol 50, 463–473.[CrossRef]
    [Google Scholar]
  24. Kumar, V., Loganathan, P., Sivaramakrishnan, G., Kriakov, J., Dusthakeer, A., Subramanyam, B., Chan, J., Jacobs, W. R., Jr & Paranji Rama, N. ( 2008; ). Characterization of temperate phage Che12 and construction of a new tool for diagnosis of tuberculosis. Tuberculosis (Edinb) 88, 616–623.[CrossRef]
    [Google Scholar]
  25. Lawrence, J. G., Hatfull, G. F. & Hendrix, R. W. ( 2002; ). Imbroglios of viral taxonomy: genetic exchange and failings of phenetic approaches. J Bacteriol 184, 4891–4905.[CrossRef]
    [Google Scholar]
  26. Lee, M. H., Pascopella, L., Jacobs, W. R., Jr & Hatfull, G. F. ( 1991; ). Site-specific integration of mycobacteriophage L5: integration- proficient vectors for Mycobacterium smegmatis, Mycobacterium tuberculosis, and bacille Calmette-Guérin. Proc Natl Acad Sci U S A 88, 3111–3115.[CrossRef]
    [Google Scholar]
  27. Marinelli, L. J., Piuri, M., Swigonova, Z., Balachandran, A., Oldfield, L., van Kessel, J. C. & Hatfull, G. F. ( 2008; ). BRED: a simple and powerful tool for constructing mutant and recombinant bacteriophage genomes. PLoS One 3, e3957 [CrossRef]
    [Google Scholar]
  28. Mediavilla, J., Jain, S., Kriakov, J., Ford, M. E., Duda, R. L., Jacobs, W. R., Jr, Hendrix, R. W. & Hatfull, G. F. ( 2000; ). Genome organization and characterization of mycobacteriophage Bxb1. Mol Microbiol 38, 955–970.
    [Google Scholar]
  29. Morris, P., Marinelli, L. J., Jacobs-Sera, D., Hendrix, R. W. & Hatfull, G. F. ( 2008; ). Genomic characterization of mycobacteriophage Giles: evidence for phage acquisition of host DNA by illegitimate recombination. J Bacteriol 190, 2172–2182.[CrossRef]
    [Google Scholar]
  30. Ojha, A. K., Baughn, A. D., Sambandan, D., Hsu, T., Trivelli, X., Guerardel, Y., Alahari, A., Kremer, L., Jacobs, W. R., Jr & Hatfull, G. F. ( 2008; ). Growth of Mycobacterium tuberculosis biofilms containing free mycolic acids and harbouring drug-tolerant bacteria. Mol Microbiol 69, 164–174.[CrossRef]
    [Google Scholar]
  31. Pedulla, M. L., Ford, M. E., Houtz, J. M., Karthikeyan, T., Wadsworth, C., Lewis, J. A., Jacobs-Sera, D., Falbo, J., Gross, J. & other authors ( 2003; ). Origins of highly mosaic mycobacteriophage genomes. Cell 113, 171–182.[CrossRef]
    [Google Scholar]
  32. Pham, T. T., Jacobs-Sera, D., Pedulla, M. L., Hendrix, R. W. & Hatfull, G. F. ( 2007; ). Comparative genomic analysis of mycobacteriophage Tweety: evolutionary insights and construction of compatible site-specific integration vectors for mycobacteria. Microbiology 153, 2711–2723.[CrossRef]
    [Google Scholar]
  33. Piuri, M. & Hatfull, G. F. ( 2006; ). A peptidoglycan hydrolase motif within the mycobacteriophage TM4 tape measure protein promotes efficient infection of stationary phase cells. Mol Microbiol 62, 1569–1585.[CrossRef]
    [Google Scholar]
  34. Piuri, M., Jacobs, W. R., Jr & Hatfull, G. F. ( 2009; ). Fluoromycobacteriophages for rapid, specific, and sensitive antibiotic susceptibility testing of Mycobacterium tuberculosis. PLoS One 4, e4870 [CrossRef]
    [Google Scholar]
  35. Sarkis, G. J. & Hatfull, G. F. ( 1998; ). Mycobacteriophages. Methods Mol Biol 101, 145–173.
    [Google Scholar]
  36. Sarkis, G. J., Jacobs, W. R., Jr & Hatfull, G. F. ( 1995; ). L5 luciferase reporter mycobacteriophages: a sensitive tool for the detection and assay of live mycobacteria. Mol Microbiol 15, 1055–1067.[CrossRef]
    [Google Scholar]
  37. Timme, T. L. & Brennan, P. J. ( 1984; ). Induction of bacteriophage from members of the Mycobacterium avium, Mycobacterium intracellulare, Mycobacterium scrofulaceum serocomplex. J Gen Microbiol 130, 2059–2066.
    [Google Scholar]
  38. van Kessel, J. C. & Hatfull, G. F. ( 2007; ). Recombineering in Mycobacterium tuberculosis. Nat Methods 4, 147–152.[CrossRef]
    [Google Scholar]
  39. van Kessel, J. C. & Hatfull, G. F. ( 2008; ). Efficient point mutagenesis in mycobacteria using single-stranded DNA recombineering: characterization of antimycobacterial drug targets. Mol Microbiol 67, 1094–1107.[CrossRef]
    [Google Scholar]
  40. van Kessel, J. C., Marinelli, L. J. & Hatfull, G. F. ( 2008; ). Recombineering mycobacteria and their phages. Nat Rev Microbiol 6, 851–857.[CrossRef]
    [Google Scholar]
  41. Xu, J., Hendrix, R. W. & Duda, R. L. ( 2004; ). Conserved translational frameshift in dsDNA bacteriophage tail assembly genes. Mol Cell 16, 11–21.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.030486-0
Loading
/content/journal/micro/10.1099/mic.0.030486-0
Loading

Data & Media loading...

Supplements

vol. , part 9, pp. 2962 - 2977

[ PDF, 316 kb]: Relationship between the genomes of BPs and TM4 Comparison of the Halo and BPs genomes where Halo gene 52 is absent from BPs



PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error