1887

Abstract

Recently, it has been shown that trehalose and mycolic acids are essential for the growth of , the causative agent of tuberculosis, and , and important but not indispensable to the survival of . Therefore, to investigate the function of mycolic acids in both the permeability of the cell wall to small nutrients and antibiotics, and the excretion of amino acids by , a trehalose-deficient mutant of the -lysine producer ATCC 21527, designated LPΔtreSΔotsAΔtreY, was constructed. By using different carbon sources in either the presence or the absence of external trehalose, a set of endogenously trehalose-free LPΔtreSΔotsAΔtreY cells that exhibited various mycolate contents was generated. The results showed that the structure of the arabinogalactan of these different cell types of LPΔtreSΔotsAΔtreY was not affected when the mycolic acid layer was either missing or impaired. Nevertheless, cells were more susceptible to antibiotics, and the permeability of their cell walls to glycerol was increased. Interestingly, a concomitant increase in the excretion of both -lysine and -glutamate was also observed, indicating that the mycolic acid content of the permeability barrier (and not only the peptidoglycan and/or the arabinogalactan) is implicated in the glutamate excretion process.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/003541-0
2007-05-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/5/1424.html?itemId=/content/journal/micro/10.1099/mic.0.2006/003541-0&mimeType=html&fmt=ahah

References

  1. Alderwick, L. J., Radmacher, E., Seidel, M., Gande, R., Hitchen, P. G., Morris, H. R., Dell, A., Sahm, H., Eggeling, L. & Besra, G. S. ( 2005; ). Deletion of Cg-emb in corynebacterianeae leads to a novel truncated cell wall arabinogalactan, whereas inactivation of Cg-ubiA results in an arabinan-deficient mutant with a cell wall galactan core. J Biol Chem 280, 32362–32371.[CrossRef]
    [Google Scholar]
  2. Bardou, F., Raynaud, C., Ramos, C., Lanéelle, M.-A. & Lanéelle, G. ( 1998; ). Mechanism of isoniazid uptake in Mycobacterium tuberculosis. Microbiology 144, 2539–2544.[CrossRef]
    [Google Scholar]
  3. Belanger, A. E., Besra, G. S., Ford, M. E., Mikusova, K., Belisle, J. T., Brennan, P. J. & Inamine, J. M. ( 1996; ). The embAB genes of Mycobacterium avium encode an arabinosyl transferase involved in cell wall arabinan biosynthesis that is the target for the antimycobacterial drug ethambutol. Proc Natl Acad Sci U S A 93, 11919–11924.[CrossRef]
    [Google Scholar]
  4. Brennan, P. J. & Nikaido, H. ( 1995; ). The envelope of mycobacteria. Annu Rev Biochem 64, 29–63.[CrossRef]
    [Google Scholar]
  5. Costa-Riu, N., Burkovski, A., Krämer, R. & Benz, R. ( 2003; ). PorA represents the major cell wall channel of the Gram-positive bacterium Corynebacterium glutamicum. J Bacteriol 185, 4779–4786.[CrossRef]
    [Google Scholar]
  6. Daffé, M. ( 2005; ). The cell envelope of corynebacteria. In Handbook of Corynebacterium glutamicum, pp. 121–148. Edited by L. Eggeling & M. Bott. Boca Raton, FL: CRC Press.
  7. Daffé, M. & Draper, P. ( 1998; ). The envelope layers of mycobacteria with reference to their pathogenicity. Adv Microb Physiol 39, 131–203.
    [Google Scholar]
  8. Daffé, M., Lanéelle, M. A., Asselineau, C., Levy-Frebault, V. & David, H. ( 1983; ). Intérêt taxonomique des acides gras des Mycobactéries: proposition d'une méthode d'analyse. Ann Microbiol 134, 241–256 (in French).
    [Google Scholar]
  9. Daffé, M., Brennan, P. J. & McNeil, M. ( 1990; ). Predominant structural features of the cell wall arabinogalactan of Mycobacterium tuberculosis as revealed through characterization of oligoglycosyl alditol fragments by gas chromatography/mass spectrometry and by 1H and 13C NMR analyses. J Biol Chem 265, 6734–6743.
    [Google Scholar]
  10. Daffé, M., McNeil, M. & Brennan, P. J. ( 1993; ). Major structural features of the cell wall arabinogalactans of Mycobacterium, Rhodococcus, and Nocardia spp. Carbohydr Res 249, 383–398.[CrossRef]
    [Google Scholar]
  11. De Smet, K. A., Weston, A., Brown, I. N., Young, D. B. & Robertson, B. D. ( 2000; ). Three pathways for trehalose biosynthesis in mycobacteria. Microbiology 146, 199–208.
    [Google Scholar]
  12. Draper, P. ( 1998; ). The outer parts of the mycobacterial envelope as permeability barriers. Frontiers Biosci 3, D1253–D1261.
    [Google Scholar]
  13. 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]
  14. Eggeling, L. & Sahm, H. ( 2003; ). The cell wall barrier of Corynebacterium glutamicum and amino acid efflux. J Biosci Bioengin 92, 201–213.
    [Google Scholar]
  15. Gande, R., Gibson, K. J., Brown, A. K., Krumbach, K., Dover, L. G., Sahm, H., Shioyama, S., Oikawa, T., Besra, G. S. & Eggeling, L. ( 2004; ). Acyl-CoA carboxylases (accD2 and accD3), together with a unique polyketide synthase (Cg-pks), are key to mycolic acid biosynthesis in Corynebacterianeae such as Corynebacterium glutamicum and Mycobacterium tuberculosis. J Biol Chem 279, 44847–44857.[CrossRef]
    [Google Scholar]
  16. Glickman, M. S., Cox, J. S. & Jacobs, W. R., Jr ( 2000; ). A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis. Mol Cell 5, 717–727.[CrossRef]
    [Google Scholar]
  17. 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]
  18. Kataoka, M., Hashimoto, K.-I., Yoshida, M., Nakamatsu, T., Horinouchi, S. & Kawasaki, H. ( 2006; ). Gene repression of Corynebacterium glutamicum in response to the conditions inducing glutamate overproduction. Lett Appl Microbiol 42, 471–476.[CrossRef]
    [Google Scholar]
  19. Kawahara, Y., Tanaka, T., Ikeda, S., Shimizu, E., Nakamatsu, T. & Nakamori, S. ( 1997; ). Relationship between the glutamate production and the activity of 2-oxoglutarate dehydrogenase in Brevibacterium lactofermentum. Biosci Biotechnol Biochem 61, 1109–1112.[CrossRef]
    [Google Scholar]
  20. Keilhauer, C., Eggeling, L. & Sahm, H. ( 1993; ). Isoleucine synthesis in Corynebacterium glutamicum: molecular analysis of the ilvB-ilvN-ilvC operon. J Bacteriol 175, 5595–5603.
    [Google Scholar]
  21. Kimura, E. ( 2005; ). l-Glutamate production. In Handbook of Corynebacterium glutamicum, pp. 439–463. Edited by E. Eggeling & M. Bott. Boca Raton, FL: CRC Press.
  22. Kwakman, J. H. & Postma, P. W. ( 1994; ). Glucose kinase has a regulatory role in carbon catabolite repression in Streptomyces coelicolor. J Bacteriol 76, 2694–2698.
    [Google Scholar]
  23. Lichtinger, T., Riess, F. G., Burkovski, A., Engelbrecht, F., Hesse, D., Kratzin, H. D., Krämer, R. & Benz, R. ( 2001; ). The low-molecular-mass subunit of the cell wall channel of the Gram-positive Corynebacterium glutamicum. Eur J Biochem 268, 462–469.
    [Google Scholar]
  24. 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]
  25. McNeil, M., Daffé, M. & Brennan, P. J. ( 1991; ). Location of the mycolyl ester substituents in the cell walls of mycobacteria. J Biol Chem 266, 13217–13223.
    [Google Scholar]
  26. Nakayama, K., Sagamihara, K. & Araki, K. ( 1973; ). Process for producing l-lysine. US patent no. 3, 708,395.
  27. Portevin, D., De Sousa-D'Auria, C., Houssin, C., Grimaldi, C., Chami, M., Daffé, M. & Guilhot, C. ( 2004; ). A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc Natl Acad Sci U S A 101, 314–319.[CrossRef]
    [Google Scholar]
  28. Portevin, D., de Sousa-D'Auria, C., Montrozier, H., Houssin, C., Stella, A., Lanéelle, M. A., Bardou, F., Guilhot, C. & Daffé, M. ( 2005; ). The acyl-AMP ligase FadD32 and AccD4-containing acyl-CoA carboxylase are required for the synthesis of mycolic acids and essential for mycobacterial growth: identification of the carboxylation product and determination of the acyl-CoA carboxylase components. J Biol Chem 280, 8862–8874.[CrossRef]
    [Google Scholar]
  29. Puech, V., Bayan, N., Salim, K., Leblon, G. & Daffé, M. ( 2000; ). Characterization of the in vivo acceptors of the mycolyl residues transferred by the corynebacterial PS1 and the related mycobacterial antigens 85. Mol Microbiol 35, 1026–1041.[CrossRef]
    [Google Scholar]
  30. Puech, V., Chami, M., Lemassu, A., Lanéelle, M. A., Schiffler, B., Gounon, P., Bayan, N., Benz, R. & Daffé, 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]
  31. Radmacher, E., Stansen, K., Besra, G. E., Alderwick, L. J., Maughan, W. N., Hollweg, G., Sahm, H., Wendisch, V. F. & Eggeling, L. ( 2005; ). Ethambutol, a cell wall inhibitor of Mycobacterium tuberculosis, elicits l-glutamate efflux of Corynebacterium glutamicum. Microbiology 151, 1359–1368.[CrossRef]
    [Google Scholar]
  32. Schäfer, A., Tauch, A., Jäger, W., Kalinowski, J., Thierbach, G. & Pühler, A. ( 1994; ). Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145, 69–73.[CrossRef]
    [Google Scholar]
  33. Sweeley, C. C., Bentley, R., Makita, M. & Wells, W. W. ( 1963; ). Gas-liquid chromatography of trimethylsilyl derivatives of sugars and related substances. J Am Chem Soc 85, 2497–2507.[CrossRef]
    [Google Scholar]
  34. Takayama, K., Armstrong, E. L., Kunugi, K. A. & Kilburn, J. O. ( 1979; ). Inhibition by ethambutol of mycolic acid transfer into the cell wall of Mycobacterium smegmatis. Agents Chemother 16, 240–242.[CrossRef]
    [Google Scholar]
  35. Tropis, M., Meniche, X., Wolf, A., Gebhardt, H., Strelkov, S., Chami, M., Schomburg, D., Krämer, R., Morbach, S. & Daffé, M. ( 2005; ). The crucial role of trehalose and structurally related oligosaccharides in the biosynthesis and transfer of mycolic acids in Corynebacterineae. J Biol Chem 280, 26573–26585.[CrossRef]
    [Google Scholar]
  36. Tzvetkov, M., Klopprogge, C., Zelder, O. & Liebl, W. ( 2003; ). Genetic dissection of trehalose biosynthesis in Corynebacterium glutamicum: inactivation of trehalose production leads to impaired growth and an altered cell wall lipid composition. Microbiology 149, 1659–1673.[CrossRef]
    [Google Scholar]
  37. Vilcheze, C., Morbidoni, H. R., Weisbrod, T. R., Iwamoto, H., Kuo, M., Sacchettini, J. C. & Jacobs, W. R., Jr ( 2000; ). Inactivation of the inhA-encoded fatty acid synthase II (FASII) enoyl–acyl carrier protein reductase induces accumulation of the FASI end products and cell lysis of Mycobacterium smegmatis. J Bacteriol 182, 4059–4067.[CrossRef]
    [Google Scholar]
  38. Wolf, A., Krämer, R. & Morbach, S. ( 2003; ). Three pathways for trehalose metabolism in Corynebacterium glutamicum ATCC13032 and their significance in response to osmotic stress. Mol Microbiol 49, 1119–1134.[CrossRef]
    [Google Scholar]
  39. York, W. S., Darwill, A. G., McNeil, M., Stevenson, J. T. & Albersheim, P. ( 1986; ). Isolation and characterization of plant cell walls and cell wall components. Methods Enzymol 118, 3–40.
    [Google Scholar]
  40. Yuan, Y., Zhu, Y., Crane, D. D. & Barry, C. E., III ( 1998; ). The effect of oxygenated mycolic acid composition on cell wall function and macrophage growth in Mycobacterium tuberculosis. Mol Microbiol 29, 1449–1458.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2006/003541-0
Loading
/content/journal/micro/10.1099/mic.0.2006/003541-0
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