1887

Abstract

Mycobacteriophages have played an important role in the development of genetic tools and diagnostics for pathogenic mycobacteria, including . However, despite the isolation of numerous phages that infect mycobacteria, the mechanisms of mycobacteriophage infection remain poorly understood, and knowledge about phage receptors is minimal. In an effort to identify the receptor for phage I3, we screened a library of transposon mutants for phage-resistant strains. All four phage I3-resistant mutants isolated were found to have transposon insertions in genes located in a cluster involved in the biosynthesis of the cell-wall-associated glycopeptidolipid (GPL), and consequently the mutants did not synthesize GPLs. The loss of GPLs correlated specifically with phage I3 resistance, as all mutants retained sensitivity to two other mycobacteriophages: D29 and Bxz1. In order to define the minimal receptor for phage I3, we then tested the phage sensitivity of previously described GPL-deficient mutants of that accumulate biosynthesis intermediates of GPLs. The results indicated that, while the removal of most sugar residues from the fatty acyl tetrapeptide (FATP) core of GPL did not affect sensitivity to phage I3, a single methylated rhamnose, transferred by the rhamnosyltransferase Gtf2 to the FATP core, was critical for phage binding.

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2009-12-01
2024-03-28
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References

  1. Ackermann H. W. 2001; Frequency of morphological phage descriptions in the year 2000. Brief review. Arch Virol 146:843–857
    [Google Scholar]
  2. 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
    [Google Scholar]
  3. 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]
  4. Barksdale L., Kim K. S. 1977; Mycobacterium . Bacteriol Rev 41:217–372
    [Google Scholar]
  5. Barsom E. K., Hatfull G. F. 1996; Characterization of Mycobacterium smegmatis gene that confers resistance to phages L5 and D29 when overexpressed. Mol Microbiol 21:159–170
    [Google Scholar]
  6. Besra G. S., Khoo K. H., Belisle J. T., McNeil M. R., Morris H. R., Dell A., Brennan P. J. 1994; New pyruvylated, glycosylated acyltrehaloses from Mycobacterium smegmatis strains, and their implications for phage resistance in mycobacteria. Carbohydr Res 251:99–114
    [Google Scholar]
  7. Billman-Jacobe H. 2004; Glycopeptidolipid synthesis in mycobacteria. Curr Sci 86:111–114
    [Google Scholar]
  8. Bisso G., Castelnuovo G., Nardelli M. G., Orefici G., Arancia G., Laneelle G., Asselineau C., Asselineau J. 1976; A study on the receptor for a mycobacteriophage: phage phlei. Biochimie 58:87–97
    [Google Scholar]
  9. Brennan P. J., Nikaido H. 1995; The envelope of mycobacteria. Annu Rev Biochem 64:29–63
    [Google Scholar]
  10. Broxmeyer L., Sosnowska D., Miltner E., Chacon O., Wagner D., McGarvey J., Barletta R. G., Bermudez L. E. 2002; Killing of Mycobacterium avium and Mycobacterium tuberculosis by a mycobacteriophage delivered by a nonvirulent mycobacterium: a model for phage therapy of intracellular bacterial pathogens. J Infect Dis 186:1155–1160
    [Google Scholar]
  11. Burguiere A., Hitchen P. G., Dover L. G., Dell A., Besra G. S. 2005; Altered expression profile of mycobacterial surface glycopeptidolipids following treatment with the antifungal azole inhibitors econazole and clotrimazole. Microbiology 151:2087–2095
    [Google Scholar]
  12. Carriere C., Riska P. F., Zimhony O., Kriakov J., Bardarov S., Burns J., Chan J., Jacobs W. R. Jr 1997; Conditionally replicating luciferase reporter phages: improved sensitivity for rapid detection and assessment of drug susceptibility of Mycobacterium tuberculosis . J Clin Microbiol 35:3232–3239
    [Google Scholar]
  13. Cirillo J. D., Barletta R. G., Bloom B. R., Jacobs W. R. Jr 1991; A novel transposon trap for mycobacteria: isolation and characterization of IS 1096 . J Bacteriol 173:7772–7780
    [Google Scholar]
  14. Dhariwal K. R., Liav A., Vatter A. E., Dhariwal G., Goren M. B. 1986; Haptenic oligosaccharides in antigenic variants of mycobacterial C-mycosides antagonize lipid receptor activity for mycobacteriophage D4 by masking a methylated rhamnose. J Bacteriol 168:283–293
    [Google Scholar]
  15. Dobson G., Minnikin D. E., Minnikin S. M., Parlett J. H., Goodfellow M., Ridell M., Magnusson M. 1985; Systematic analysis of complex mycobacterial lipids. In Chemical Methods in Bacterial Systematics pp 237–265 Edited by Goodfellow M., Minnikin D. E. London: Academic Press;
    [Google Scholar]
  16. Estrela A. I., Pooley H. M., de Lencastre H., Karamata D. 1991; Genetic and biochemical characterization of Bacillus subtilis 168 mutants specifically blocked in the synthesis of the teichoic acid poly(3- O- β-d-glucopyranosyl- N-acetylgalactosamine 1-phosphate): gneA, a new locus, is associated with UDP- N-acetylglucosamine 4-epimerase activity. J Gen Microbiol 137:943–950
    [Google Scholar]
  17. Froman S., Will D. W., Bogen E. 1954; Bacteriophage active against virulent Mycobacterium tuberculosis. I. Isolation and activity. Am J Public Health Nations Health 44:1326–1333
    [Google Scholar]
  18. Furuchi A., Tokunaga T. 1972; Nature of the receptor substance of Mycobacterium smegmatis for D4 bacteriophage adsorption. J Bacteriol 111:404–411
    [Google Scholar]
  19. Hatfull G. H. 2005; Mycobacteriophages and tuberculosis. In Tuberculosis and the Tubercle Bacillus pp 203–218 Edited by Cole S. T., Eisenach D., McMurray D. N., Jacobs W. R. Jr Washington, DC: American Society for Microbiology;
    [Google Scholar]
  20. Hatfull G. F., Jacobs W. R. Jr 1994; Mycobacteriophages: cornerstones of mycobacterial research. In Tuberculosis: Pathogenesis, Protection and Control pp 165–183 Edited by Bloom B. R. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  21. Hazbon M. H., Guarin N., Ferro B. E., Rodriguez A. L., Labrada L. A., Tovar R., Riska P. F., Jacobs W. R. Jr 2003; Photographic and luminometric detection of luciferase reporter phages for drug susceptibility testing of clinical Mycobacterium tuberculosis isolates. J Clin Microbiol 41:4865–4869
    [Google Scholar]
  22. Heller K. J. 1992; Molecular interaction between bacteriophage and the gram-negative cell envelope. Arch Microbiol 158:235–248
    [Google Scholar]
  23. Herrero M., de Lorenzo V., Timmis K. N. 1990; Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172:6557–6567
    [Google Scholar]
  24. Jacobs W. R. Jr, Kalpana G. V., Cirillo J. D., Pascopella L., Snapper S. B., Udani R. A., Jones W., Barletta R. G., Bloom B. R. 1991; Genetic systems for mycobacteria. Methods Enzymol 204:537–555
    [Google Scholar]
  25. 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
    [Google Scholar]
  26. Kriakov J., Lee S., Jacobs W. R. Jr 2003; Identification of a regulated alkaline phosphatase, a cell surface-associated lipoprotein, in Mycobacterium smegmatis . J Bacteriol 185:4983–4991
    [Google Scholar]
  27. Kubica G. P. 1982; Phage typing of Mycobacterium tuberculosis: a time for standardization. Am Rev Respir Dis 126:3–4
    [Google Scholar]
  28. Larsen M. H., Biermann K., Tandberg S., Hsu T., Jacobs W. R. Jr 2007; Genetic manipulation of Mycobacterium tuberculosis . Curr Protoc Microbiol Chapter 10: Unit 10A.2
    [Google Scholar]
  29. Lee S., Kriakov J., Vilcheze C., Dai Z., Hatfull G. F., Jacobs W. R. Jr 2004; Bxz1, a new generalized transducing phage for mycobacteria. FEMS Microbiol Lett 241:271–276
    [Google Scholar]
  30. Mankiewicz E., Beland J. 1964; The role of mycobacteriophages and of cortisone in experimental tuberculosis and sarcoidosis. Am Rev Respir Dis 89:707–720
    [Google Scholar]
  31. McAdam R. A., Quan S., Smith D. A., Bardarov S., Betts J. C., Cook F. C., Hooker E. U., Lewis A. P., Woollard P. other authors 2002; Characterization of a Mycobacterium tuberculosis H37Rv transposon library reveals insertions in 351 ORFs and mutants with altered virulence. Microbiology 148:2975–2986
    [Google Scholar]
  32. McNerney R., Traore H. 2005; Mycobacteriophage and their application to disease control. J Appl Microbiol 99:223–233
    [Google Scholar]
  33. Miyamoto Y., Mukai T., Nakata N., Maeda Y., Kai M., Naka T., Yano I., Makino M. 2006; Identification and characterization of the genes involved in glycosylation pathways of mycobacterial glycopeptidolipid biosynthesis. J Bacteriol 188:86–95
    [Google Scholar]
  34. 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
    [Google Scholar]
  35. 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
    [Google Scholar]
  36. 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
    [Google Scholar]
  37. Rado T. A., Bates J. H., Engel H. W., Mankiewicz E., Murohashi T., Mizuguchi Y., Sula L. 1975; World Health Organization studies on bacteriophage typing of mycobacteria. Subdivision of the species Mycobacterium tuberculosis . Am Rev Respir Dis 111:459–468
    [Google Scholar]
  38. Raj C. V., Ramakrishnan T. 1970; Transduction in Mycobacterium smegmatis . Nature 228:280–281
    [Google Scholar]
  39. Ramesh G. R., Gopinathan K. P. 1994; Structural proteins of mycobacteriophage I3: cloning, expression and sequence analysis of a gene encoding a 70 kDa structural protein. Gene 143:95–100
    [Google Scholar]
  40. Riska P. F., Su Y., Bardarov S., Freundlich L., Sarkis G., Hatfull G., Carrière C., Kumar V., Chan J., Jacobs W. R. Jr 1999; Rapid film-based determination of antibiotic susceptibilities of Mycobacterium tuberculosis strains by using a luciferase reporter phage and the Bronx Box. J Clin Microbiol 37:1144–1149
    [Google Scholar]
  41. Sampson T., Broussard G. W., Marinelli L. J., Jacobs-Sera D., Ray M., Ko C. C., Russell D., Hendrix R. W., Hatfull G. F. 2009; Mycobacteriophages BPs, Angel, and Halo: comparative genomics reveals a novel class of ultra small mobile genetic elements. Microbiology 155:2962–2977
    [Google Scholar]
  42. Schorey J. S., Sweet L. 2008; The mycobacterial glycopeptidolipids: structure, function, and their role in pathogenesis. Glycobiology 18:832–841
    [Google Scholar]
  43. Snapper S. B., Lugosi L., Jekkel A., Melton R. E., Kieser T., Bloom B. R., Jacobs W. R. Jr 1988; Lysogeny and transformation in mycobacteria: stable expression of foreign genes. Proc Natl Acad Sci U S A 85:6987–6991
    [Google Scholar]
  44. Snapper S. B., Melton R. E., Mustafa S., Kieser T., Jacobs W. R. Jr 1990; Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis . Mol Microbiol 4:1911–1919
    [Google Scholar]
  45. Tran H. L., Fiedler F., Hodgson D. A., Kathariou S. 1999; Transposon-induced mutations in two loci of Listeria monocytogenes serotype 1/2a result in phage resistance and lack of N-acetylglucosamine in the teichoic acid of the cell wall. Appl Environ Microbiol 65:4793–4798
    [Google Scholar]
  46. van Kessel J. C., Marinelli L. J., Hatfull G. F. 2008; Recombineering mycobacteria and their phages. Nat Rev Microbiol 6:851–857
    [Google Scholar]
  47. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119
    [Google Scholar]
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