1 The Global Architecture of the Mycobacterial Cell Envelope

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

1 The Global Architecture of the Mycobacterial Cell Envelope, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815783/9781555814687_Chap01-1.gif /docserver/preview/fulltext/10.1128/9781555815783/9781555814687_Chap01-2.gif


The cell envelope of mycobacteria, i.e., the compounds that surround the cytoplasm and protect the micro-organisms from their environment, is important for the bacterial physiology because inhibition of the production of some of its constituents, e.g., mycolic acids and arabinogalactan, kills the cells. It is also this structure that controls the transfer of materials into and out of the mycobacterium. The wall possesses a fundamental, covalently linked “cell-wall skeleton” (CWS) associated with a great variety of noncovalently linked substances, of which a majority are lipids and glycolipids. Isolated plasma membranes are typically obtained by breaking the cells by mechanical stress, e.g., sonication or shearing in the French pressure cell, followed by fractionation using differential centrifugation or density gradients. The wall of mycobacteria consists of a covalently linked CWS, and an abundant variety of wall-associated lipids and a few polypeptides. That the outermost layer of the mycobacterial cell envelope is partly polysaccharide in nature could be deduced from the staining of electron-transparent zone (ETZ) with peroxidase-conjugated concanavalin A and from old data showing that mycobacterial culture filtrates, notably the preparation called tuberculin, contain several polysaccharides. The polysaccharide/protein matrix in pathogens would also serve as a defense mechanism by facilitating survival in the host. The capsule and its constituents can also act by actively modifying the behavior of host cells in some way beneficial to the bacterium, as recently shown for the glucan from .

Citation: Daffé M. 2008. 1 The Global Architecture of the Mycobacterial Cell Envelope, p 3-11. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch1

Key Concept Ranking

Cell Wall Proteins
Plasma Membrane
Cell Wall Components
Transmission Electron Microscopy
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1.
Figure 1.

Electron micrograph of the cell envelope of mycobacteria. Left: ultrathin section of fixed with glutaraldehyde and lysine in buffer containing ruthenium red and postfixed with osmium tetroxide; bacteria were suspended in uranyl acetate, and cells were embedded in agar before dehydration with ethanol. Right: interpretation of the image showing the proposed arrangement of plasma membrane, hypothetical periplasm, cell wall core components (peptidoglycan, arabinogalactan, mycolic acids) and associated (extractable) lipids, and outer layer (called the “capsule” in the case of pathogenic species). Note that proteins are not represented in this figure, with notable exception of the cell wall pore-forming proteins (porins). This model of the arrangement of the mycobacterial cell envelope is based on that of Minnikin ( ), modified by Daffé and Draper ( ).

Citation: Daffé M. 2008. 1 The Global Architecture of the Mycobacterial Cell Envelope, p 3-11. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch1
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Akamatsu, Y.,, Y. Ono, and, S. Nojima. 1966. Phospholipid patterns in subcellular fractions of Mycobacterium phlei. J. Biochem. (Tokyo) 59:176182.
2. Amar-Nacasch, C., and, E. Vilkas. 1970. Étude des parois de Mycobacterium tuberculosis. II. Mise en évidence d’un mycolate d’arabinobiose et d’un glucane dans les parois de M. tuberculosis H37Ra. Bull. Soc. Chim. Biol. 52:145151.
3. Asselineau, C.,, S. Clavel,, F. Clément,, M. Daffé,, H. L. David,, M.-A. Lanéelle, and, J.-C. Promé. 1981. Constituants lipidiques de Mycobacterium leprae isolé de tatou infecté expérimentalement. Ann. Microbiol. (Inst. Pasteur) 132A:1930.
4. Barksdale, L. and, K.-S. Kim. 1977. Mycobacterium. Bacteriol. Rev. 41:217372.
5. Benedetti, E., L., L. Dunia,, M. A. Ludosky,, N. V. Man,, D. D. Trach,, N. Rastogi, and, H. L. David. 1984. Freeze-etching and freeze-fracture structural features of cell envelopes in mycobacteria and leprosy derived corynebacteria. Acta Leprol. 95:237248.
6. Bloch, H. and, H. Noll. 1953. Studies on the virulence of tubercle bacilli. Variation in virulence effected by Tween 80 and thiosemicarbazone. J. Exp. Med. 97:116.
7. Boddingius, J. and, H. Dijkman. 1990. Subcellular localization of Mycobacterium leprae-specific phenolic glycolipid (PGL-I) antigen in human leprosy lesions and in M. leprae isolated from armadillo liver. J. Gen. Microbiol. 136:20012012.
8. Brodie, A. F.,, S.-H. Lee, and, V. K. Kalra. 1979. Transport and energy transduction mechanism in Mycobacterium phlei, p. 46–53. In D. Schlessinger (ed.), Microbiology. ASM, Washington, DC.
9. Chapman, G. B.,, J. H. Hanks, and, J. H. Wallace. 1959. An electron microscope study of the disposition and fine structure of Mycobacterium lepraemurium in mouse spleen. J. Bacteriol. 77:205211.
10. Daffé, M., and, P. Draper. 1998. The envelope layers of mycobacteria with reference to their pathogenicity. Adv. Microb. Physiol. 39:131203.
11. Daffé, M., and, G. Etienne. 1999. The capsule of Mycobacterium tuberculosis and its implications for pathogenicity. Tuberc. Lung Dis. 79:153169.
12. Daffé, M.,, C. Lacave,, M.-A. Lanéelle, and, G. Lanéelle. 1987. Structure of the major triglycosyl phenol-phthiocerol of Mycobacterium tuberculosis (strain Canetti). Eur. J. Biochem. 167:155160.
13. Daffé, M.,, M.-A. Dupont, and, N. Gas. 1989. The cell envelope of Mycobacterium smegmatis: cytochemistry and architectural implications. FEMS Microbiol. Lett. 61:8994.
14. Daffé, M.,, P. J. Brennan, and, M. McNeil. 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. 265:67346743.
15. Daffé, M.,, P. J. Brennan, and, M. McNeil. 1993. Major structural features of the cell wall arabinogalactans of Mycobacterium, Rhodococcus, and Nocardia spp. Carbohydr. Res. 249:383398.
16. Daniel, T. M. 1984. Soluble mycobacterial antigens, p. 417–465. In G. P. Kubica and, L. G. Wayne (ed.), The Mycobacteria: a Sourcebook, part A. Marcel Dekker, Inc, New York, NY.
17. Dinadayala, P.,, F. Laval,, C. Raynaud,, A. Lemassu,, M. A. Lanéelle,, G. Lanéelle, and, M. Daffé. 2003. Tracking the putative precursors of oxygenated mycolates of Mycobacterium tuberculosis. Structural analysis of fatty acids of a mutant devoid of methoxy-and ketomycolates. J. Biol Chem. 278:73107319.
18. Draper, P. 1971. The walls of Mycobacterium lepraemurium: chemistry and ultrastructure. J. Gen. Microbiol. 69:313332.
19. Draper, P. 1998. The outer parts of the mycobacterial envelope as permeability barriers. Front. Biosci. 3:D1253D1261.
20. Fréhel, C.,, A. Ryter,, N. Rastogi, and, H. L. David. 1986. The electron-transparent zone in phagocytised Mycobacterium avium and other mycobacteria: formation, persistence and role in bacterial survival. Ann. Inst. Pasteur/Microbiol. 137B:239257.
21. Fréhel, C.,, N. Rastogi,, J.-C. Bénichou, and, A. Ryter. 1988. Do test tube-grown pathogenic mycobacteria possess a protective capsule? FEMS Microbiol. Lett. 56:225230.
22. Gagliardi, M. C.,, L. Lemassu,, R. Teloni,, S. Mariotti,, V. Sargentini,, M. Pardini,, M. Daffé, and, R. Nisini. Cell-wall associated alpha-glucan is instrumental for Mycobacterium tuberculosis to block CD1 molecule expression and disable the function of dendritic cell derived from infected monocyte. Cell Microbiol. 3:20812092.
23. Goldman, D. S. 1970. Subcellular localization of individual mannose-containing phospholipids in Mycobacterium tuberculosis. Am. Rev. Respir. Dis. 102:543555.
24. Goren, M. B., and, P. J. Brennan. 1979. Mycobacterial lipids: chemistry and biologic activities, p. 63–193. In G. P. Youmans (ed.), Tuberculosis. W. B. Saunders Company, Philadelphia, PA.
25. Hanks, J. H. 1961a. Capsules in electron micrographs of Mycobacterium leprae. Int. J. Lepr. 29:8487.
26. Hanks, J. H. 1961b. The problem of preserving internal structures in pathogenic mycobacteria by conventional methods of fixation. Int. J. Lepr. 29:175178.
27. Hanks, J. H. 1961c. Demonstration of capsules on M. leprae during carbol-fuchsin staining mechanism of the Ziehl-Neelsen stain. Int. J. Lepr. 26:179182.
28. Hanks, J. H. 1961d. The origin of the capsules on Mycobacterium leprae and other tissue-grown mycobcteria. Int. J. Lepr. 26:172174.
29. Hanks, J. H.,, J. T. Moore, and, J. E. Michaels. 1961. Significance of capsular components of Mycobacterium leprae and other mycobacteria. Int. J. Lepr. 26:7483.
30. Hunter, S. W., and, P. J. Brennan. 1990. Evidence for the presence of a phosphatidylinositol anchor on the lipoarabinomannan and lipomannan of Mycobacterium tuberculosis. J. Biol. Chem. 265:92729279.
31. Hunter, S. W.,, H. Gaylord, and, P. J. Brennan. 1986. Structure and antigenicity of the phosphorylated lipopolysaccharides from the leprosy and tubercle bacilli. J. Biol. Chem. 261:1234512351.
32. Jarlier, V., and, H. Nikaido, 1990. Permeability barrier to hydrophilic solutes in Mycobacterium chelonei (sic). J. Bacteriol. 172:14181423.
33. Kent, P. W. 1951. Structure of an antigenic polysaccharide isolated from tuberculin. J. Chem. Soc. 1:364368.
34. Kondo, E., and, K. Kanai. 1976. A suggested role of a host-parasite lipid complex in mycobacterial infection. Jpn. J. Med. Sci. Biol. 29:199210.
35. Kotani, S.,, T. Kitaura,, T. Hirano, and, A. Tanaka. (1959). Isolation and chemical composition of the cells walls of BCG. Biken J. 2:129141.
36. Kumar, G.,, V. K. Kalra, and, A. F. Brodie. 1979. Asymmetric distribution of phospholipids in membranes from Mycobacterium phlei. Arch. Biochem. Biophys. 198:2230.
37. Lanéelle, M. A.,, D. Promé,, G. Lanéelle, and, J. C. Promé. 1990. Ornithine lipid of Mycobacterium tuberculosis: its distribution in some slow- and fast-growing mycobacteria. J. Gen. Microbiol. 136:773778.
38. Lemassu, A., and, M. Daffé. 1994. Structural features of the exocellular polysaccharides of Mycobacterium tuberculosis. Biochem. J. 297:351357.
39. Lemassu, A.,, A. Ortalo-Magné,, F. Bardou,, G. Silve,, M. A. Lanéelle, and, M. Daffé. 1996. Extracellular and surface-exposed polysaccharides of non-tuberculous mycobacteria. Microbiology 142:15131520.
40. Liu, J.,, E. Y. Rosenberg, and, H. Nikaido, 1995. Fluidity of the lipid domain of cell wall from Mycobacterium chelonae. Proc. Natl. Acad. Sci. USA 92:1125411258.
41. McNeil, M.,, M. Daffé, and, P. J. Brennan. 1990. Evidence for the nature of the link between the arabinogalactan and peptidoglycan of mycobacterial cell walls. J. Biol. Chem. 265:1820018206.
42. McNeil, M.,, M. Daffé, and, P. J. Brennan 1991. Location of the mycoloyl ester substituents in the cell walls of mycobacteria. J. Biol. Chem. 266:1321713223.
43. McNeil, M. R., and, P. J. Brennan. 1991. Structure, function and biogenesis of the cell envelope of mycobacterial in relation to bacterial physiology, pathogenesis and drug resistance; some thoughts and possibilities arising from recent structural information. Res. Microbiol. 142:451463.
44. Middlebrook, G.,, R. J. Dubos, and, C. Pierce. 1947. Virulence and morphological characteristics of mammalian tubercle bacilli. J. Exp. Med. 86:175184.
45. Minnikin, D. E. 1982. Lipids: complex lipids, their chemistry, biosynthesis and roles, p. 95–184. In C. Ratledge and, J. Stanford (ed.), The Biology of the Mycobacteria, vol. 1. Physiology, Identification and Classification. Academic Press, London, United Kingdom.
46. Misaki, A., and, S. Yukawa. 1966. Studies on cell walls of Mycobacteria. II. Constitution of polysaccharides from BCG cell walls. J. Biochem. 59:511520.
47. Nikaido, H.,, S.-H. Kim, and, E. Y. Rosenberg. 1993. Physical organization of lipids in the cell wall of Mycobacterium chelonae. Mol. Microbiol. 8:10251030.
48. Oka, S.,, K. Fukushi,, M. Fujimoto,, H. Sato, and, M. Motomiya. 1968. La distribution subcellulaire des phospholipides de la mycobactérie. C. R. Soc. Franco-Jpn. Biol. 162:16481650.
49. Ortalo-Magné, A.,, M.-A. Dupont,, A. Lemassu,, Å. B. Andersen,, P. Gounon, and, M. Daffé. 1995. Molecular composition of the outermost capsular material of the tubercle bacillus. Microbiology 141:16091620.
50. Ortalo-Magné, A.,, Å. B. Andersen, and, M. Daffé, 1996a. The outermost capsular arabinomannans and other mannoconjugates of virulent and avirulent tubercle bacilli. Microbiology 142:927935.
51. Ortalo-Magné, A.,, A. Lemassu,, M. A. Lanéelle,, F. Bardou,, G. Silve,, P. Gounon,, G. Marchal, and, M. Daffé. 1996b. Identification of the surface-exposed lipids on the cell envelope of Mycobacterium tuberculosis and other mycobacterial species. J. Bacteriol. 178:456461.
52. Paul, T. R., and, T. J. Beveridge. 1992. Reevaluation of envelope profiles and cytoplasmic ultrastructure of mycobacteria processed by conventional embedding and freeze-substitution protocols. J. Bacteriol. 174:65086517.
53. Paul, T. R., and, T. J. Beveridge. 1994. Preservation of surface lipids and determination of ultrastructure of Mycobacterium kansasii by freeze-substitution. Infect. Immun. 62:15421550.
54. Picard, B.,, C. Frehel, and, N. Rastogi. 1984. Cytochemical characterization of mycobacterial outer surfaces. Acta Leprol. 95:227235.
55. Puech, V.,, M. Chami,, A. Lemassu,, M. A. Lanéelle,, B. Schiffler,, P. Gounon,, N. Bayan,, R. Benz, and, M. Daffé. 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 147:13651382.
56. Rambukkana, A.,, P. K. A. Das,, A. Chand,, J. G. Baas,, D. G. Groothuis, and, A. H. J. Kolk. 1991. Subcellular distribution of monoclonal antibody defined epitopes on immunodominant Mycobacterium tuberculosis proteins in the 30-kDa region: identification and localization of 29/33-kDa doublet proteins on mycobacterial cell wall. Scand. J. Immunol. 33:763775.
57. 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. 142:464476.
58. Rastogi, N.,, V. Lévy-Frebault,, M. C. Blom-Potar, and, H. L. David. 1989. Ability of smooth and rough variants of Mycobacterium avium and M. intracellulare to multiply and survive intracellularly: role of C-mycosides. Zentbl. Bakteriol. Mikrobiol. Hyg. 270:345360.
59. Raynaud, C.,, G. Etienne,, P. Peyron,, M.-A. Lanéelle, and, M. Daffé. 1998. Extracellular enzyme activities potentially involved in the pathogenicity of Mycobacterium tuberculosis. Microbiology 144:577587.
60. Rezwan, M.,, M.-A. Lanéelle,, P. Sander, and, M. Daffé. 2007. Breaking down the wall: fractionation of mycobacteria. J. Microbiol. Methods 68:3239.
61. Rulong, S.,, A. P. Aguas,, P. P. Da Silva, and, T. S. Silva. 1991. Intramacrophagic Mycobacterium avium bacilli are coated by a multiple lamellar structure: freeze fracture analysis of infected mouse liver. Infect. Immun. 59:38953902.
62. Ryter, A.,, C. Fréhel,, N. Rastogi, and, H. L. David. 1984. Macrophage interaction with mycobacteria including M. leprae. Acta Leprol. 95:211235.
63. Schwebach, J.,, A. Glatman-Freedman,, L. Gunter-Cummins,, Z. Dai,, J. Robbins,, R. Schneerson, and, A. Casadevall, 2002. Glucan is a component of the Mycobacterium tuberculosis surface that is expressed in vitro and in vivo. Infect. Immun. 70:25662575.
64. Seibert, F. B. 1949. The isolation of three different proteins and two polysaccharides from tuberculin by alcohol fractionation. Their chemical and biological properties. Am. Rev. Tuberc. 59:86101.
65. Seibert, F. B.,, M. Stacey, and, P. W. Kent. 1949. An antigenic polysaccharide, “polysaccharide II” isolated from tuberculin. Biochim. Biophys. Acta 3:632640.
66. Senaratne, R. H.,, H. Mobasheri,, K. G. Papavininasasundaram,, P. Jenner,, E. J. A. Lea, and, P. Draper. 1998. Expression of a gene for a porin-like protein of the OmpA family from Mycobacterium tuberculosis H37Rv. J. Bacteriol. 180:35413547.
67. Silva, M. T., and, P. M. Macedo. 1983a. A comparative ultrastructural study of the membranes of Mycobacterium leprae and of cultivable Mycobacteria (sic). Biol. Cell. 47:383386.
68. Silva, M. T., and, P. M. Macedo. 1983b. The interpretation of the ultrastructure of mycobacterial cells in transmission electron microscopy in ultrathin sections. Int. J. Lepr. 51:225234.
69. Silva, M. T., and, P. M. Macedo. 1984. Ultrastructural characterization of normal and damaged membranes of Mycobacterium leprae and cultivable mycobacteria. J. Gen. Microbiol. 130:369380.
70. Silva, M.T.,, F. Portaels, and, P. M. Macedo. 1989. New data on the ultrastructure of the membrane of Mycobacterium leprae. Int. J. Lepr. 57:5464.
71. Sonnenberg, M. G., and, J. T. Belisle. 1997. Definition of Mycobacterium tuberculosis culture filtrate proteins by two-dimensional polyacrylamide gel electrophoresis, N-terminal amino-acid sequencing and electrospray mass spectrometry. Infect. Immun. 65:45154524.
72. Trias, J., and, R. Benz. 1993. Characterization of the channel formed by the mycobacterial porin in lipid bilayer membranes. Demonstration of voltage gating and of negative point charges at the channel mouth. J. Biol. Chem. 268:62346240.
73. Trias, J.,, V. Jarlier, and, R. Benz. 1992. Porins in the cell wall of mycobacteria. Science 258:14791481.
74. Wiker, H. G.,, M. Harboe, and, S. Nagai. 1991. A localization index for distinction between extracellular and intracellular antigens of Mycobacterium tuberculosis. J. Gen. Microbiol. 137:875884.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error