1887

Abstract

Members of the complex are distinguished by the presence of highly antigenic surface molecules called glycopeptidolipids (GPLs) and the oligosaccharide portion of the serovar-specific GPL defines the 28 serovars. Previously, the genomic region () encoding the enzymes responsible for the glycosylation of the lipopeptide core to generate the serovar-2-specific GPLs has been described. In this work, the gene clusters of serovar 2 strains 2151 and TMC 724 were fully sequenced and compared to the homologous regions of serovar 1 strain 104, subsp. and subsp. . It was also determined that 104Rg, a mutant of strain 104 that produces truncated GPLs, lost several GPL biosynthesis genes by deletion. This comparison, together with analysis of protein similarities, supports a biosynthetic model in which serovar-2-specific GPLs are synthesized from a serovar-1-specific GPL intermediate that is derived from a non-specific GPL precursor. We also identified a gene encoding an enzyme that is necessary for the biosynthesis of serovar-3- and 9-specific GPLs, but not serovar-2-specific GPLs, suggesting that the different serovars may have evolved from the acquisition or loss of genetic information. In addition, a subcluster of genes for the biosynthesis and transfer of fucose, which are needed to make serovar-specific GPLs such as those of serovar 2, is found in the non-GPL-producing subspecies and .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26528-0
2003-10-01
2021-03-07
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/10/mic1492797.html?itemId=/content/journal/micro/10.1099/mic.0.26528-0&mimeType=html&fmt=ahah

References

  1. Andrianopoulos K., Wang L., Reeves P. R. 1998; Identification of the fucose synthetase gene in the colanic acid gene cluster of Escherichia coli K-12. J Bacteriol 180:998–1001
    [Google Scholar]
  2. Arakawa Y., Wacharotayankun R., Nagatsuka T., Ito H., Kato N., Ohta M. 1995; Genomic organization of the Klebsiella pneumoniae cps region responsible for serotype K2 capsular polysaccharide synthesis in the virulent strain Chedid. J Bacteriol 177:1788–1796
    [Google Scholar]
  3. Aspinall G. O., Chatterjee D., Brennan P. J. 1995; The variable surface glycolipids of mycobacteria: structures, synthesis of epitopes, and biological properties. Adv Carbohydr Chem Biochem 51:169–242
    [Google Scholar]
  4. Belisle J. T., Pascopella L., Inamine J. M., Brennan P. J., Jacobs W. R. Jr 1991; Isolation and expression of a gene cluster responsible for biosynthesis of the glycopeptidolipid antigens of Mycobacterium avium . J Bacteriol 173:6991–6997
    [Google Scholar]
  5. Belisle J. T., McNeil M. R., Chatterjee D., Inamine J. M., Brennan P. J. 1993a; Expression of the core lipopeptide of the glycopeptidolipid surface antigens in rough mutants of Mycobacterium avium . J Biol Chem 268:10510–10516
    [Google Scholar]
  6. Belisle J. T., Klaczkiewicz K., Brennan P. J., Jacobs W. R. Jr, Inamine J. M. 1993b; Rough morphological variants of Mycobacterium avium . Characterization of genomic deletions resulting in the loss of glycopeptidolipid expression. J Biol Chem 268:10517–10523
    [Google Scholar]
  7. Brennan P. J. 1988; Mycobacterium and other actinomycetes. In Microbial Lipids vol. 1 pp  203–298 Edited by Ratledge C., Wilkinson S. G. London: Academic Press;
    [Google Scholar]
  8. Brennan P. J., Goren M. B. 1979; Structural studies on the type-specific antigens and lipids of the Mycobacterium aviumMycobacterium intracellulareMycobacterium scrofulaceum serocomplex. J Biol Chem 254:4205–4211
    [Google Scholar]
  9. Bull T. J., Sheridan J. M., Martin H., Sumar N., Tizard M., Hermon-Taylor J. 2000; Further studies on the GS element: a novel mycobacterial insertion sequence (IS 1612 ), inserted into an acetylase gene ( mpa ) in Mycobacterium avium subsp. silvaticum but not in Mycobacterium avium subsp. paratuberculosis . Vet Microbiol 77:453–563
    [Google Scholar]
  10. Chatterjee D., Khoo K.-H. 2001; The surface glycopeptidolipids of mycobacteria: structures and biological properties. Cell Mol Life Sci 58:2018–2042
    [Google Scholar]
  11. Clarke B. R., Pearce R., Roberts I. S. 1999; Genetic organization of the Escherichia coli K10 capsule gene cluster: identification and characterization of two conserved regions in Group III capsule gene clusters encoding polysaccharide transport functions. J Bacteriol 181:2279–2285
    [Google Scholar]
  12. Cole S. T., Brosch R., Parkhill J. 39 other authors 1998; Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537–544
    [Google Scholar]
  13. Corpet F. 1988; Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:10881–10890
    [Google Scholar]
  14. Eckstein T. M., Silbaq F. S., Chatterjee D., Kelly N. J., Brennan P. J., Belisle J. T. 1998; Identification and recombinant expression of a Mycobacterium avium rhamnosyltransferase gene ( rtfA) involved in glycopeptidolipid biosynthesis. J Bacteriol 180:5567–5573
    [Google Scholar]
  15. Eckstein T. M., Inamine J. M., Lambert M. L., Belisle J. T. 2000; A genetic mechanism for the deletion of the ser2 gene cluster and formation of rough morphological variants of Mycobacterium avium . J Bacteriol 182:6177–6182
    [Google Scholar]
  16. Eiglmeier K., Honore N., Woods S. A., Caudron B., Cole S. T. 1993; Use of an ordered cosmid library to deduce the genomic organization of Mycobacterium leprae . Mol Microbiol 7:197–206
    [Google Scholar]
  17. Florido M., Appelberg R., Orme I. M., Cooper A. M. 1997; Evidence for a reduced chemokine response in the lungs of beige mice infected with Mycobacterium avium . Immunology 90:600–606
    [Google Scholar]
  18. Hashimoto Y., Li N., Yokoyama H., Ezaki T. 1993; Complete nucleotide sequence and molecular characterization of ViaB region encoding Vi antigen in Salmonella typhi . J Bacteriol 175:4456–4465
    [Google Scholar]
  19. Henderson I. R., Nataro J. P. 1999; A conserved motif in the hexosyltransferases. Mol Microbiol 33:222
    [Google Scholar]
  20. Hilt W., Pfleiderer G., Fortnagel P. 1991; Glucose dehydrogenase from Bacillus subtilis expressed in Escherichia coli . I: purification, characterization and comparison with glucose dehydrogenase from Bacillus megaterium . Biochim Biophys Acta 1076:298–304
    [Google Scholar]
  21. Ibrahim R. K., Bruneau A., Bantignies B. 1998; Plant O -methyltransferases: molecular analysis, common signature and classification. Plant Mol Biol 36:1–10
    [Google Scholar]
  22. Inouye M., Suzuki H., Takada Y., Muto N., Horinouchi S., Beppu T. 1994; A gene encoding mycinamicin III O -methyltransferase from Micromonospora griseorubida . Gene 141:121–124
    [Google Scholar]
  23. Ishikawa J., Hotta K. 1999; FramePlot: a new implementation of the Frame analysis for predicting protein-coding regions in bacterial DNA with a high G+C content. FEMS Microbiol Lett 174:251–253
    [Google Scholar]
  24. Jeevarajah D., Patterson J. H., McConville M. J., Billman-Jacobe H. 2002; Modification of glycopeptidolipids by an O -methyltransferase of Mycobacterium smegmatis . Microbiology 148:3079–3087
    [Google Scholar]
  25. Kroll J. S. 1992; The genetics of encapsulation in Haemophilus influenzae . J Infect Dis 165:Suppl. 1S93–S96
    [Google Scholar]
  26. Krzywinska E., Schorey J. S. 2003; Characterization of genetic differences between Mycobacterium avium subsp. avium strains of diverse virulence with a focus on the glycopeptidolipid biosynthesis cluster. Vet Microbiol 91:249–264
    [Google Scholar]
  27. Mahairas G. G., Sabo P. J., Hickey M. J., Singh D. C., Stover C. K. 1996; Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis . J Bacteriol 178:1274–1282
    [Google Scholar]
  28. Maslow J. N., Dawson D., Carlin E. A., Holland S. M. 1999; Hemolysin as a virulence factor for systemic infection with isolates of Mycobacterium avium complex. J Clin Microbiol 37:445–446
    [Google Scholar]
  29. Mills J. A., McNeil M. R., Belisle J. T., Jacobs W. R. Jr, Brennan P. J. 1994; Loci of Mycobacterium avium ser2 gene cluster and their functions. J Bacteriol 176:4803–4808
    [Google Scholar]
  30. Patterson J. H., McConville M. J., Coppel R. L., Billman-Jacobe H. 2000; Identification of a methyltransferase from Mycobacterium smegmatis involved in glycopeptidolipid synthesis. J Biol Chem 275:24900–24906
    [Google Scholar]
  31. Pedrosa J., Florido M., Kunze Z. M., Castro A. G., Portaels F., McFadden J., Silva M. T., Appelberg R. 1994; Characterization of the virulence of Mycobacterium avium complex (MAC) isolates in mice. Clin Exp Immunol 98:210–216
    [Google Scholar]
  32. Rahn A., Drummelsmith J., Whitfield C. 1999; Conserved organization in the cps gene clusters for expression of Escherichia coli group 1 K antigens: relationship to the colanic acid biosynthesis locus and the cps genes from Klebsiella pneumoniae . J Bacteriol 181:2307–2313
    [Google Scholar]
  33. Recht J., Kolter R. 2001; Glycopeptidolipid acetylation affects sliding motility and biofilm formation in Mycobacterium smegmatis . J Bacteriol 183:5718–5724
    [Google Scholar]
  34. Recht J., Martínez A., Torello S., Kolter R. 2000; Genetic analysis of sliding motility in Mycobacterium smegmatis . J Bacteriol 182:4348–4351
    [Google Scholar]
  35. Slauch J. M., Lee A. A., Mahan M. J., Mekalanos J. J. 1996; Molecular characterization of the oafA locus responsible for acetylation of Salmonella typhimurium O-antigen: OafA is a member of a family of integral membrane trans-acylases. J Bacteriol 178:5904–5909
    [Google Scholar]
  36. Stevenson G., Andrianopoulos K., Hobbs M., Reeves P. R. 1996; Organization of the Escherichia coli K-12 gene cluster responsible for production of the extracellular polysaccharide colanic acid. J Bacteriol 178:4885–4893
    [Google Scholar]
  37. Tizard M., Bull T., Millar D., Doran T., Martin H., Sumar N., Ford J., Hermon-Taylor J. 1998; A low G+C content genetic island inMycobacterium avium subsp. paratuberculosis and M. avium subsp. silvaticum with homologous genes in Mycobacterium tuberculosis . Microbiology 144:3413–3423
    [Google Scholar]
  38. Torrelles J. B., Ellis D., Osborne T., Hoefer A., Orme I. M., Chatterjee D., Brennan P. J., Cooper A. M. 2002; Characterization of virulence, colony morphotype and glycopeptidolipid of Mycobacterium avium strain 104. Tuberculosis 82:293–300
    [Google Scholar]
  39. van Schie B. J., Hellingwerf K. J., van Dijken J. P., Elferink M. G., van Dijl J. M., Kuenen J. G., Konings W. N. 1985; Energy transduction by electron transfer via a pyrrolo-quinoline quinone-dependent glucose dehydrogenase in Escherichia coli , Pseudomonas aeruginosa , and Acinetobacter calcoaceticus (var. lwoffi) . J Bacteriol 163:493–499
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26528-0
Loading
/content/journal/micro/10.1099/mic.0.26528-0
Loading

Data & Media loading...

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