1887

Abstract

Modified -cyclodextrins have been shown previously to enhance sterol conversion to 4-androstene-3,17-dione (AD) and 1,4-androstadiene-3,17-dione (ADD) by growing spp. The enhancement effect was mainly attributed to steroid solubilization by the formation of inclusion complexes with modified cyclodextrins. In this work, the influence of randomly methylated -cyclodextrin (MCD) on the growth, AD- and ADD-producing activity, cell wall (CW) composition and ultrastructure of sterol-transforming sp. VKM Ac-1816D was studied. The specific growth rate of the strain on glycerol increased in the presence of MCD (20–100 mM). Washed cells grown in the presence of MCD (20–40 mM) expressed 1.6-fold higher ADD-producing activity than did the cells grown without MCD, and their adhesiveness differed. Electron microscopy showed MCD-mediated CW exfoliation and accumulation of membrane-like structures outside the cells, while preserving cells intact. The analysis of CW composition revealed both a decrease in the proportion of extractable lipids and a considerable shift in fatty acid profile resulting from MCD action. The MCD-mediated enhancement of mycolic and fatty acids content was observed outside the cells. The total secreted protein level rose 2.4-fold, and the extracellular 3-hydroxysteroid oxidase activity 3.2-fold. The composition of the CW polysaccharide was not altered, while the overall proportion of the carbohydrates in the CW of the MCD-exposed mycobacteria increased. The results showed that the multiple mechanisms of MCD-mediated intensification of sterol to AD(D) conversion by mycobacteria include not only solubilization of steroids, but also the increase of CW permeability for both steroids and soluble nutrients, disorganization of the lipid bilayer and the release of steroid-transforming enzymes weakly associated with the CW.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/001636-0
2007-06-01
2019-11-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/6/1981.html?itemId=/content/journal/micro/10.1099/mic.0.2006/001636-0&mimeType=html&fmt=ahah

References

  1. Atrat, P., Hosel, P., Richter, W., Meyer, H. W. & Hörhold, C. ( 1991; ). Interactions of Mycobacterium fortuitum with solid substrate particles. J Basic Microbiol 31, 413–422.[CrossRef]
    [Google Scholar]
  2. Bendinger, B., Rijnaarts, H. H. M., Altendorf, K. & Zehnder, A. J. B. ( 1993; ). Physicochemical cell surface and adhesive properties of coryneform bacteria related to the presence and chain length of mycolic acids. Appl Environ Microbiol 59, 3973–3977.
    [Google Scholar]
  3. Borrego, S., Niubo, E., Ancheta, O. & Espinosa, M. E. ( 2000; ). Study of the microbial aggregation in Mycobacterium using image analysis and electron microscopy. Tissue Cell 32, 494–500.[CrossRef]
    [Google Scholar]
  4. Bradford, M. M. ( 1976; ). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248–254.[CrossRef]
    [Google Scholar]
  5. Brennan, P. J. & Nikaido, H. ( 1995; ). The envelope of mycobacteria. Annu Rev Biochem 64, 29–63.[CrossRef]
    [Google Scholar]
  6. Chatterjee, D. ( 1997; ). The mycobacterial cell wall: structure, biosynthesis and sites of drug action. Curr Opin Chem Biol 1, 579–588.[CrossRef]
    [Google Scholar]
  7. Daffe, M. & Draper, P. ( 1998; ). The envelope layers of mycobacteria with reference to their pathogenicity. Adv Microb Physiol 39, 131–203.
    [Google Scholar]
  8. Donova, M. V., Dovbnya, D. V. & Koshcheyenko, K. A. ( 1996; ). Modified CDs-mediated enhancement of microbical sterol sidechain degradation. In Proceedings of the eighth International Symposium on Cyclodextrins, pp. 527–530. Dordrecht: Kluwer Publishers.
  9. Draper, P. ( 1982; ). The anatomy of mycobacteria. In The Biology of the Mycobacteria, vol. 1, part 1, pp. 9–49. Edited by C. Ratledge & J. Stanford. London/New York: Academic Press.
  10. Dubnau, E., Chan, J., Raynaud, C., Mohan, V. P., Laneelle, M. A., Yu, K., Quemaard, A., Smith, I. & Daffe, M. ( 2000; ). Oxygenated mycolic acids are necessary for virulence of Mycobacterium tuberculosis in mice. Mol Microbiol 36, 630–637.
    [Google Scholar]
  11. Etienne, G., Villeneuve, C., Billman-Jacobe, H., Astarie-Dequeker, C., Dupont, M.-A. & Daffe, M. ( 2002; ). The impact of the absence of glycopeptolipids on the ultrastructure, cell surface and cell wall properties, and phagocytosis of Mycobacterium smegmatis.. Microbiology 148, 3089–3100.
    [Google Scholar]
  12. Fromming, K.-H. & Szejtly, J. ( 1993; ). Cyclodextrins in pharmacy. In Topics in Inclusion Science, vol. 5, pp. 1–81. Edited by J. E. D. Davies. Dordrecht: Kluwer Academic Publishers.
  13. Greenberg-Ofrath, N., Terespolosky, Y., Kahane, Y. & Bar, R. ( 1993; ). Cyclodextrins as carriers of cholesterol and fatty acids in cultivation of mycoplasmas. Appl Environ Microbiol 59, 547–551.
    [Google Scholar]
  14. Haberland, M. E. & Reynolds, J. A. ( 1973; ). Self-association of cholesterol in aqueous solution. Proc Natl Acad Sci U S A 70, 2313–2316.[CrossRef]
    [Google Scholar]
  15. Hesselink, P. G. M., van Vliet, S., de Vries, H. & Witholt, B. ( 1989; ). Optimization of steroid side-chain cleavage by Mycobacterium sp. in the presence of cyclodextrins. Enzyme Microb Technol 11, 398–404.[CrossRef]
    [Google Scholar]
  16. Jadoun, J. & Bar, R. ( 1993; ). Microbial transformations in a cyclodextrin medium. Part 4. Enzyme vs microbial oxidation of cholesterol. Appl Microbiol Biotechnol 40, 477–482.
    [Google Scholar]
  17. Jarlier, V. & Nikaido, H. ( 1994; ). Mycobacterial cell wall: structure and role in natural resistance to antibiotics. FEMS Microbiol Lett 123, 11–18.[CrossRef]
    [Google Scholar]
  18. Khomutov, S. M., Sukhodoloskaya, G. V. & Donova, M. V. ( 2001; ). Cyclodextrin stabilization of steroid against microbial degradation. . Biological Journal of Armenia (Special issue Cyclodextrin) 53, 194–200 (in Russian).
    [Google Scholar]
  19. Khomutov, S. M., Sidorov, I. A., Dovbnya, D. V. & Donova, M. V. ( 2002; ). Estimation of cyclodextrin affinity to steroids. J Pharm Pharmacol 54, 617–622.[CrossRef]
    [Google Scholar]
  20. Korycka-Machala, M., Ziolkowski, A., Rumijowska-Galewicz, A., Lisowska, K. & Sedlaczek, L. ( 2001; ). Polycations increase the permeability of Mycobacterium vaccae cell envelopes to hydrophobic compounds. Microbiology 147, 2769–2781.
    [Google Scholar]
  21. Lacave, C., Lanelle, M. A. & Lanelle, G. ( 1990; ). Mycolic acid synthesis by Mycobacterium aurum cell free extracts. Biochim Biophys Acta 1042, 315–323.[CrossRef]
    [Google Scholar]
  22. Lisowska, K., Korycka, M., Hadlaw-Klimaszewska, O., Ziolkowski, A. & Sedlaczek, L. ( 1996; ). Permeability of mycobacterium cell envelopes to sterols: peptidoglycan as the diffusion barrier. J Basic Microbiol 36, 407–419.[CrossRef]
    [Google Scholar]
  23. Liu, J., Barry, C. E., III, 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]
  24. Matsuyama, K., El-Gizawy, S. & Perrin, J. ( 1987; ). Thermodynamics of binding of amino acids to α-, β- and γ-cyclodextrins. Drug Dev Ind Pharm 13, 2687–2689.[CrossRef]
    [Google Scholar]
  25. Minnikin, D. E. ( 1991; ). Chemical principles in the organization of the lipid components in the mycobacterial cell envelope. Res Microbiol 142, 423–427.[CrossRef]
    [Google Scholar]
  26. Nikaido, H. & Jarlier, V. ( 1991; ). Permeability of the mycobacterial cell wall. Res Microbiol 142, 437–443.[CrossRef]
    [Google Scholar]
  27. Nikolayeva, V. M., Egorova, O. V., Dovbnya, D. V. & Donova, M. V. ( 2004; ). Extracellular 3β-hydroxysteroid oxidase of Mycobacterium vaccae VKM Ac-1815 D. J Steroid Biochem Mol Biol 91, 79–85.[CrossRef]
    [Google Scholar]
  28. Puech, V., Chami, M., Lemassu, A., Laneelle, M.-A., Schiffler, B., Gounon, P., Bayan, N., Benz, R. & Daffe, M. ( 2001; ). Structure of the cell envelope of corynebacteria: importance of the non-covalently bound lipids in the formation of the cell wall permeability barrier and fracture plane. Microbiology 147, 1365–1382.
    [Google Scholar]
  29. Ratledge, C. ( 1982; ). Lipids: cell composition, fatty acid biosynthesis. In The Biology of the Mycobacteria, vol. 1, part 1, pp. 53–93. Edited by C. Ratledge & J. Stanford. London & New York: Academic Press.
  30. Reynolds, E. S. ( 1963; ). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17, 208–213.[CrossRef]
    [Google Scholar]
  31. Rumijowska, A., Lisowska, K., Ziolkovski, A. & Sedlaczek, L. ( 1997; ). Transformation of sterols by Mycobacterium vaccae: effects of lecithin on the permeability of cell envelopes to sterols. World J Microbiol Biotechnol 13, 89–95.[CrossRef]
    [Google Scholar]
  32. Schimz, K.-L., Irrgang, K. & Overhoff, B. ( 1985; ). Trehalose, a cytoplasmic reserve disaccharide of Cellulomonas sp. DSM20108: its identification, carbon-source-dependent accumulation, and degradation during starvation. FEMS Microbiol Lett 30, 165–169.[CrossRef]
    [Google Scholar]
  33. Sedlaczek, L., Gorminski, B. M. & Lisowska, K. ( 1994; ). Effect of inhibitors of cell envelope synthesis on β-sitosterol sidechain degradation by Mycobacterium sp. NRRL MB 3683. J Basic Microbiol 34, 387–399.[CrossRef]
    [Google Scholar]
  34. Sedlaczek, L., Lisowska, K., Korycka, M., Rumijowska, A., Ziolkowski, A. & Dlugonski, J. ( 1999; ). The effect of cell wall components on glycine-enhanced sterol side chain degradation to androstene derivatives by mycobacteria. Appl Microbiol Biotechnol 52, 563–571.[CrossRef]
    [Google Scholar]
  35. Sojo, M., Bru, R., Lopez-Molina, D., Garcia-Carmona, F. & Argulles, J.-C. ( 1997; ). Cell-linked and extracellular cholesterol oxidase activities from Rhodococcus erythropolis. Isolation and physiological characterization. Appl Microbiol Biotechnol 47, 583–589.[CrossRef]
    [Google Scholar]
  36. Szejtli, J. ( 1997; ). Utilization of cyclodextrins in industrial products and processes. J Mater Chem 7, 575–587.[CrossRef]
    [Google Scholar]
  37. Szentirmai, A. ( 1990; ). Microbial physiology of side chain degradation of steroids. J Ind Microbiol Biotechnol 6, 101–115.
    [Google Scholar]
  38. Trias, J. & Benz, R. ( 1994; ). Permeability of the cell wall of Mycobacterium smegmatis.. Mol Microbiol 14, 283–290.[CrossRef]
    [Google Scholar]
  39. Trias, J., Jarlier, V. & Benz, R. ( 1992; ). Porins in the cell wall of mycobacteria. Science 258, 1479–1481.[CrossRef]
    [Google Scholar]
  40. Wang, L., Slayden, R. A., Barry, C. E., III & Liu, J. ( 2000; ). Cell wall structure of a mutant of Mycobacterium smegmatis defective in the biosynthesis of mycolic acids. J Biol Chem 275, 7224–7229.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2006/001636-0
Loading
/content/journal/micro/10.1099/mic.0.2006/001636-0
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