1887

Abstract

is often used as a surrogate host for pathogenic mycobacteria, especially since the isolation of the transformable smooth morphotype strain mc155 from the isogenic rough wild-type strain ATCC 607. Biochemical analysis of the cell envelope components revealed a lack of polar glycolipids, namely the lipooligosaccharides and the polar subfamilies of glycopeptidolipids, in the mc155 strain. In addition, the latter strain differs from its parent by the distribution of various species of glycolipids and phospholipids between the outermost and deeper layers of the cell envelope. The presence of filamentous and rope-like structures at the cell surface of mc155 cells grown in complex media further supported an ultrastructural change in the cell envelope of the mutant. Importantly, a significantly more rapid uptake of the hydrophobic chenodeoxycholate was observed for the mutant compared to wild-type cells. Taken together, these data indicate that the nature of the surface-exposed and envelope constituents is crucial for the surface properties, cell wall permeability and bacterial phenotype, and suggest that the transformable character of the mc155 strain may be in part explained by these profound modifications of its cell envelope.

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2005-06-01
2019-10-18
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References

  1. 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 51, 169–242.
    [Google Scholar]
  2. Bardou, F., Raynaud, C., Ramos, C., Lanéelle, M.-A. & Lanéelle, G. ( 1998; ). Isoniazid uptake mechanism in Mycobacterium tuberculosis. Microbiology 144, 2539–2544.[CrossRef]
    [Google Scholar]
  3. Barrow, W. W. & Brennan, P. J. ( 1982; ). Isolation in high frequency of rough variants of Mycobacterium intracellulare lacking C-mycoside glycopeptidolipid antigens. J Bacteriol 150, 381–384.
    [Google Scholar]
  4. Bayer, M. E. & Sloyer, J. L. ( 1990; ). The electrophoretic mobility of Gram-negative and Gram-positive bacteria: an electrokinetic analysis. J Gen Microbiol 136, 867–874.[CrossRef]
    [Google Scholar]
  5. Behr, M. A., Wilson, M. A., Gill, W. P., Salamon, H., Schoolnik, G. K., Rane, S. & Small, P. M. ( 1999; ). Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 28, 1520–1523.
    [Google Scholar]
  6. 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]
  7. Belisle, J. T., Klaczkiewicz, K., Brennan, P. J., Jacobs, W. R. & Inamine, J. M. ( 1993b; ). Rough morphological variants of Mycobacterium avium. J Biol Chem 268, 10517–10523.
    [Google Scholar]
  8. Billman-Jacobe, H., McConville, M. J., Haites, R. E., Kovacevic, S. & Coppel, R. L. ( 1999; ). Identification of a peptide synthetase involved in the biosynthesis of glycopeptidolipids of Mycobacterium smegmatis. Mol Microbiol 33, 1244–1253.
    [Google Scholar]
  9. Brennan, P. J. ( 1988; ). Mycobacterium and other actinomycetes. In Microbial Lipids, vol. 1, pp. 251–278. Edited by C. Ratledge & S. G. Wilkinson. London: Academic Press.
  10. Brennan, P. J. & Nikaido, H. ( 1995; ). The envelope of mycobacteria. Annu Rev Biochem 64, 29–63.[CrossRef]
    [Google Scholar]
  11. Brosch, R., Gordon, S. V., Marmiesse, M. & 12 other authors ( 2002; ). A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci U S A 99, 3684–3689.[CrossRef]
    [Google Scholar]
  12. Camacho, L. R., Constant, P., Raynaud, C., Lanéelle, M.-A., Triccas, J. A., Gicquel, B., Daffé, M. & Guilhot, C. ( 2001; ). Analysis of the phthiocerol dimycocerosate locus of Mycobacterium tuberculosis. Evidence that this lipid is involved in the cell wall permeability barrier. J Biol Chem 276, 19845–19854.[CrossRef]
    [Google Scholar]
  13. Cangelosi, G. A., Palermo, C. O., Laurent, J.-P., Hamlin, A. M. & Brabant, W. H. ( 1999; ). Colony morphotypes on Congo red agar segregate along species and drug susceptibility lines in the Mycobacterium avium–intracellulare complex. Microbiology 145, 1317–1324.[CrossRef]
    [Google Scholar]
  14. Chatterjee, D. & Khoo, K.-H. ( 2001; ). The surface glycopeptidolipids of mycobacteria: structures and biological properties. Cell Mol Life Sci 58, 2018–2042.[CrossRef]
    [Google Scholar]
  15. Cougoule, C., Constant, P., Etienne, G., Daffé, M. & Maridonneau-Parini, I. ( 2002; ). Lack of fusion of azurophil granules with phagosomes during phagocytosis of Mycobacterium smegmatis by human neutrophils is not actively controlled by the bacteria. Infect Immun 70, 1591–1598.[CrossRef]
    [Google Scholar]
  16. Daffé, M. & Draper, P. ( 1998; ). The envelope layers of mycobacteria with reference to their pathogenicity. Adv Microb Physiol 39, 131–201.
    [Google Scholar]
  17. Daffé, M. & Lemassu, A. ( 2000; ). Glycobiology of the mycobacterial surface. Structures and biological activities of the cell envelope glycoconjugates. In Glycomicrobiology, pp. 225–273. Edited by R. J. Doyle. New York: Kluwer Academic/Plenum.
  18. Daffé, M., Lanéelle, M.-A., Asselineau, C., Lévy-Frébault, V. & David, H. ( 1983a; ). Intérêt taxonomique des acides gras des mycobactéries: proposition d'une méthode d'analyse. Ann Microbiol 134B, 579–584.
    [Google Scholar]
  19. Daffé, M., Lanéelle, M.-A. & Puzo, G. ( 1983b; ). Structural elucidation by field desorption and electron-impact mass spectrometry of the C-mycosides isolated from Mycobacterium smegmatis. Biochim Biophys Acta 751, 439–443.[CrossRef]
    [Google Scholar]
  20. Daffé, M., Dupont, M.-A. & Gas, N. ( 1989; ). The cell envelope of Mycobacterium smegmatis: cytochemistry and architectural implications. FEMS Microbiol Lett 61, 89–94.[CrossRef]
    [Google Scholar]
  21. Daffé, M., McNeil, M. & Brennan, P. J. ( 1991; ). Novel type-specific lipoologosaccharides from Mycobacterium tuberculosis. Biochemistry 30, 378–388.[CrossRef]
    [Google Scholar]
  22. Dische, Z. ( 1962; ). Color reaction of hexoses. Methods Carbohydr Chem 1, 488–494.
    [Google Scholar]
  23. Draper, P. ( 1982; ). The anatomy of mycobacteria. In The Biology of the Mycobacteria, vol. 1, pp. 9–49. Edited by C. Ratledge & J. L. Stanford. London: Academic Press.
  24. Dubnau, E., Chan, J., Raynaud, C., Mohan, V. P., Lanéelle, M.-A., Yu, K., Quemard, A., Smith, I. & Daffé, M. ( 2000; ). Oxygenated mycolic acids are necessary for virulence of Mycobacterium tuberculosis in mice. Mol Microbiol 36, 630–637.
    [Google Scholar]
  25. Eckstein, T. M., Inamine, J. M., Lambert, M. L. & Belisle, J. T. ( 2000; ). A genetic mechanism for deletion of the ser2 gene cluster and formation of rough morphological variants of Mycobacterium avium. J Bacteriol 182, 6177–6182.[CrossRef]
    [Google Scholar]
  26. Etienne, G., Villeneuve, C., Billman-Jacobe, H., Astarie-Dequeker, C., Dupont, M.-A. & Daffé, M. ( 2002; ). The impact of the absence of glycopeptidolipids on the ultrastructure, cell surface and cell wall properties, and phagocytosis of Mycobacterium smegmatis. Microbiology 148, 3089–3100.
    [Google Scholar]
  27. Furuchi, A. & Tokunaga, T. ( 1972; ). Nature of the receptor substance of Mycobacterium smegmatis for D4 bacteriophage adsorption. J Bacteriol 111, 404–411.
    [Google Scholar]
  28. Galamba, A., Soetaert, K., Wang, X.-M., De Bruyn, J., Jacobs, P. & Content, J. ( 2001; ). Disruption of adhC reveals a large duplication in the Mycobacterium smegmatis mc2155 genome. Microbiology 147, 3281–3294.
    [Google Scholar]
  29. George, K. M., Yuan, Y., Sherman, D. R. & Barry, C. E. ( 1995; ). The biosynthesis of cyclopropanated mycolic acids in Mycobacterium tuberculosis. Identification and functional analysis of cma-2. J Biol Chem 270, 27292–27298.[CrossRef]
    [Google Scholar]
  30. Gordon, S. V., Brosch, R., Billault, A., Garnier, T., Eiglmeier, K. & Cole, S. T. ( 1999; ). Identification of variable regions in the genomes of tubercle bacilli using bacterial artificial chromosome arrays. Mol Microbiol 32, 643–655.[CrossRef]
    [Google Scholar]
  31. Goren, M. B., McClatchy, J. K., Martens, B. & Brokl, O. ( 1972; ). Mycosides C: behavior as receptor site substance for mycobacteriophage D4. J Virol 9, 999–1003.
    [Google Scholar]
  32. Howard, S. T., Byrd, T. F. & Lyons, C. R. ( 2002; ). A polymorphic region in Mycobacterium abscessus contains a novel insertion sequence element. Microbiology 148, 2987–2996.
    [Google Scholar]
  33. Jackson, M., Raynaud, C., Lanéelle, M.-A., Guilhot, C., Laurent-Winter, C., Ensergueix, D., Gicquel, B. & Daffé, M. ( 1999; ). Inactivation of the antigen 85C gene profoundly affects the mycolate content and alters the permeability of the Mycobacterium tuberculosis cell envelope. Mol Microbiol 31, 1573–1587.[CrossRef]
    [Google Scholar]
  34. Jacobs, W. R., Jr ( 2000; ). Mycobacterium tuberculosis: a once genetically intractable organism. In Molecular Genetics of Mycobacteria, pp. 1–16. Edited by G. F. Hatfull & W. R. Jacobs, Jr. Washington, DC: American Society for Microbiology.
  35. Kamisango, K., Saada, S., Dell, A. & Ballou, C. E. ( 1985; ). Pyruvylated glycolipids from Mycobacterium smegmatis. Nature and location of the lipid components. J Biol Chem 260, 4117–4121.
    [Google Scholar]
  36. Laval, F., Lanéelle, M. A., Déon, C., Monsarrat, B. & Daffé, M. ( 2001; ). Accurate molecular mass determination of mycolic acids by MALDI-TOF mass spectrometry. Anal Chem 73, 4537–4544.[CrossRef]
    [Google Scholar]
  37. Lemassu, A., Vincent Lévy-Frébault, V., Lanéelle, M.-A. & Daffé, M. ( 1992; ). Lack of correlation between colony morphology and lipooligosaccharide content in the Mycobacterium tuberculosis complex. J Gen Microbiol 138, 1535–1541.[CrossRef]
    [Google Scholar]
  38. Lemassu, A., Ortalo-Magné, A., Bardou, F., Silve, G., Lanéelle, M.-A. & Daffé, M. ( 1996; ). Extracellular and surface-exposed polysaccharides of non-tuberculous mycobacteria. Microbiology 142, 1513–1520.[CrossRef]
    [Google Scholar]
  39. Liu, J., Rosenberg, E. Y. & Nikaido, H. ( 1995; ). Fluidity of the lipid domain of cell wall from Mycobacterium chelonae. Proc Natl Acad Sci U S A 92, 11254–11258.[CrossRef]
    [Google Scholar]
  40. Liu, J., Barry, C. E., Besra, G. S. & Nikaido, H. ( 1996; ). Mycolic acid structure determines the fluidity of the mycobacterial cell wall. J Biol Chem 271, 29545–29551.[CrossRef]
    [Google Scholar]
  41. Martinez, A., Torello, S. & Kolter, R. ( 1999; ). Sliding motility in mycobacteria. J Bacteriol 181, 7331–7338.
    [Google Scholar]
  42. Minnikin, D. E. ( 1982; ). Lipids: complex lipids, their chemistry, biosynthesis and roles. In The Biology of the Mycobacteria, vol. 1, pp. 95–184. Edited by C. Ratledge & J. L. Stanford. London: Academic Press.
  43. Minnikin, D. E., Minnikin, S. M., Parlett, J. H., Goodfellow, M. & Magnusson, M. ( 1984; ). Mycolic acid patterns of some species of Mycobacterium. Arch Microbiol 139, 225–231.
    [Google Scholar]
  44. Moormann, M., Zähringer, U., Moll, H., Kaufmann, R., Schmid, R. & Altendorf, K. ( 1997; ). A new glycosylated lipopeptide incorporated into the cell wall of a smooth variant of Gordona hydrophobica. J Biol Chem 272, 10729–10738.[CrossRef]
    [Google Scholar]
  45. Ojha, A. K., Varma, S. & Chatterji, D. ( 2002; ). Synthesis of an unusual polar glycopeptidolipid in glucose-limited culture of Mycobacterium smegmatis. Microbiology 148, 3039–3048.
    [Google Scholar]
  46. Ortalo-Magné, A., Dupont, M.-A., Lemassu, A., Andersen, A. B., Gounon, P. & Daffé, M. ( 1995; ). Molecular composition of the outermost capsular material of the tubercle bacillus. Microbiology 141, 1609–1620.[CrossRef]
    [Google Scholar]
  47. Ortalo-Magné, A., Lemassu, A., Lanéelle, M.-A., Bardou, F., Silve, G., Gounon, P., Marchal, G. & Daffé, M. ( 1996; ). Identification of the surface-exposed lipids on the cell envelope of Mycobacterium tuberculosis and other mycobacterial species. J Bacteriol 178, 456–461.
    [Google Scholar]
  48. O'Shea, B., Khare, S., Bliss, K., Klein, P., Ficht, T. A., Adams, L. G. & Rice-Ficht, A. C. ( 2004; ). Amplified fragment length polymorphism reveals genomic variability among Mycobacterium avium subsp. paratuberculosis isolates. J Clin Microbiol 42, 3600–3606.[CrossRef]
    [Google Scholar]
  49. Paul, T. R. & Beveridge, T. J. ( 1992; ). Reevaluation of envelope profiles and cytoplasmic ultrastructure of mycobacteria processed by conventional embedding and freeze-substitution protocols. J Bacteriol 174, 6508–6517.
    [Google Scholar]
  50. Rastogi, N. ( 1991; ). Recent observations concerning structure and function relationships in the mycobacterial cell envelope: elaboration of a model in terms of mycobacterial pathogenicity, virulence and drug-resistance. Res Microbiol 142, 464–476.[CrossRef]
    [Google Scholar]
  51. Rastogi, N., Fréhel, C. & David, H. L. ( 1984; ). Cell envelope architectures of leprosy-derived corynebacteria, Mycobacterium leprae, and related organisms: a comparative study. Curr Microbiol 11, 23–30.[CrossRef]
    [Google Scholar]
  52. Rastogi, N., Fréhel, C. & David, H. L. ( 1986; ). Triple-layered structure of mycobacterial cell wall: evidence for the existence of a polysaccharide-rich outer layer in 18 mycobacterial species. Curr Microbiol 13, 237–242.[CrossRef]
    [Google Scholar]
  53. Raynaud, C., Etienne, G., Peyron, P., Lanéelle, M.-A. & Daffé, M. ( 1998; ). Extracellular enzyme activities potentially involved in the pathogenicity of Mycobacterium tuberculosis. Microbiology 144, 577–587.[CrossRef]
    [Google Scholar]
  54. Recht, J. & Kolter, R. ( 2001; ). Glycopeptidolipid acetylation affects sliding motility and biofilm formation in Mycobacterium smegmatis. J Bacteriol 183, 5718–5724.[CrossRef]
    [Google Scholar]
  55. Recht, J., Martinez, A., Torello, S. & Kolter, R. ( 2000; ). Genetic analysis of sliding motility in Mycobacterium smegmatis. J Bacteriol 182, 4348–4351.[CrossRef]
    [Google Scholar]
  56. Rosenberg, M., Gutnick, D. & Rosenberg, E. ( 1980; ). Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 9, 29–33.[CrossRef]
    [Google Scholar]
  57. Saada, S. & Ballou, C. E. ( 1983; ). Pyruvylated glycolipids from Mycobacterium smegmatis. Structures of two oligosaccharides components. J Biol Chem 258, 1813–1818.
    [Google Scholar]
  58. 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.[CrossRef]
    [Google Scholar]
  59. Sreevatsan, S., Pan, X., Stockbauer, K. E., Connell, N. D., Kreiswirth, B. N., Whittam, T. S. & Musser, J. M. ( 1997; ). Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc Natl Acad Sci U S A 94, 9869–9874.[CrossRef]
    [Google Scholar]
  60. Tsolaki, A. G., Hirsh, A. E., DeRiemer, K. & 7 other authors ( 2004; ). Functional and evolutionary genomics of Mycobacterium tuberculosis: insights from genomic deletions in 100 strains. Proc Natl Acad Sci U S A 101, 4865–4870.[CrossRef]
    [Google Scholar]
  61. Villeneuve, C., Etienne, G., Abadie, V., Montrozier, H., Bordier, C., Laval, F., Daffé, M., Maridonneau-Parini, I. & Astarie-Dequeker, C. ( 2003; ). Surface-exposed glycopeptidolipids of Mycobacterium smegmatis specifically inhibit the phagocytosis of mycobacteria by human macrophages. Identification of a novel family of glycopeptidolipids. J Biol Chem 278, 51291–51300.[CrossRef]
    [Google Scholar]
  62. Yuan, Y., Crane, D. C., Musser, J. M., Sreevatsan, S. & Barry, C. E., 3rd ( 1997; ). MMAS-1, the branch point between cis- and trans-cyclopropane-containing oxygenated mycolates in Mycobacterium tuberculosis. J Biol Chem 272, 10041–10049.[CrossRef]
    [Google Scholar]
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