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Unraveling the Structure of the Mycobacterial Envelope

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  • Authors: Mamadou Daffé1, Hedia Marrakchi2
  • Editors: Vincent A. Fischetti3, Richard P. Novick4, Joseph J. Ferretti5, Daniel A. Portnoy6, Miriam Braunstein7, Julian I. Rood8
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Institut de Pharmacologie et de Biologie Structurale, Université de Toulouse, CNRS, UPS, Department of Tuberculosis and Infection Biology, Toulouse, France; 2: Institut de Pharmacologie et de Biologie Structurale, Université de Toulouse, CNRS, UPS, Department of Tuberculosis and Infection Biology, Toulouse, France; 3: The Rockefeller University, New York, NY; 4: Skirball Institute for Molecular Medicine, NYU Medical Center, New York, NY; 5: Department of Microbiology & Immunology, University of Oklahoma Health Science Center, Oklahoma City, OK; 6: Department of Molecular and Cellular Microbiology, University of California, Berkeley, Berkeley, CA; 7: Department of Microbiology and Immunology, University of North Carolina-Chapel Hill, Chapel Hill, NC; 8: Infection and Immunity Program, Monash Biomedicine Discovery Institute, Monash University, Melbourne, Australia
  • Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0027-2018
  • Received 23 March 2018 Accepted 23 March 2019 Published 05 July 2019
  • Mamadou Daffé, [email protected]
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  • Abstract:

    The mycobacterial cell envelope consists of a typical plasma membrane of lipid and protein surrounded by a complex cell wall composed of carbohydrate and lipid. In pathogenic species, such as , an outermost “capsule” layer surrounds the cell wall. This wall embraces a fundamental, covalently linked “cell-wall skeleton” composed of peptidoglycan, solidly attached to arabinogalactan, whose penta-saccharide termini are esterified by very-long-chain fatty acids (mycolic acids). These fatty acids form the inner leaflet of an outer membrane, called the mycomembrane, whose outer leaflet consists of a great variety of non-covalently linked lipids and glycolipids. The thickness of the mycomembrane, which is similar to that of the plasma membrane, is surprising in view of the length of mycoloyl residues, suggesting dedicated conformations of these fatty acids. Finally, a periplasmic space also exists in mycobacteria, between the plasma membrane and the peptidoglycan. This article provides a comprehensive overview of this biologically important and structurally unique mycobacterial cell compartment.

  • Citation: Daffé M, Marrakchi H. 2019. Unraveling the Structure of the Mycobacterial Envelope. Microbiol Spectrum 7(4):GPP3-0027-2018. doi:10.1128/microbiolspec.GPP3-0027-2018.

References

1. Wayne LG, Kubica GP. 1986. The mycobacteria, p 1435–1457. In Sneath PHA, Mair NS, Sharpe ME, Holt JG (ed), Bergey’s Manual of Systematic Bacteriology. Williams & Wilkins, Baltimore, MD.
2. Touchette MH, Seeliger JC. 2017. Transport of outer membrane lipids in mycobacteria. Biochim Biophys Acta Mol Cell Biol Lipids 1862:1340–1354 http://dx.doi.org/10.1016/j.bbalip.2017.01.005. [PubMed]
3. Goren MB, Brennan PJ. 1979. Tuberculosis, p 63–193. In Youmans GP (ed), Mycobacterial Lipids: Chemistry and Biologic Activities. W.B. Saunders Company, Philadelphia, PA.
4. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, Quail MA, Rajandream MA, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537–544. [PubMed]
5. Jankute M, Cox JAG, Harrison J, Besra GS. 2015. Assembly of the mycobacterial cell wall. Annu Rev Microbiol 69:405–423 http://dx.doi.org/10.1146/annurev-micro-091014-104121. [PubMed]
6. Daffé M, Quémard A, Marrakchi H. 2018. Mycolic acids: from chemistry to biology. In Geiger O (ed), Biogenesis of Fatty Acids, Lipids and Membranes. Handbook of Hydrocarbon and Lipid Microbiology Series. Springer, Cham, Switzerland.
7. Chalut C. 2016. MmpL transporter-mediated export of cell-wall associated lipids and siderophores in mycobacteria. Tuberculosis (Edinb) 100:32–45 http://dx.doi.org/10.1016/j.tube.2016.06.004. [PubMed]
8. Gröschel MI, Sayes F, Simeone R, Majlessi L, Brosch R. 2016. ESX secretion systems: mycobacterial evolution to counter host immunity. Nat Rev Microbiol 14:677–691 http://dx.doi.org/10.1038/nrmicro.2016.131. [PubMed]
9. Daffé M, Draper P. 1998. The envelope layers of mycobacteria with reference to their pathogenicity. Adv Microb Physiol 39:131–203 http://dx.doi.org/10.1016/S0065-2911(08)60016-8.
10. Daffé M, Zuber B. 2014. The fascinating coat surrounding mycobacteria. p 179–192. In Remaut H, Fronzes R (ed), Bacterial Membranes: Structural and Molecular Biology, Caister Academic Press, Poole, UK.
11. Zuber B, Chami M, Houssin C, Dubochet J, Griffiths G, Daffé M. 2008. Direct visualization of the outer membrane of native mycobacteria and corynebacteria. J Bacteriol 190:5672–5680 http://dx.doi.org/10.1128/JB.01919-07. [PubMed]
12. Daffé M, Dupont MA, Gasc N. 1989. The cell envelope of Mycobacterium smegmatis: cytochemistry and architectural implications. FEMS Microbiol Lett 52:89–93 http://dx.doi.org/10.1111/j.1574-6968.1989.tb03558.x.
13. Silva MT, Macedo PM. 1983. A comparative ultrastructural study of the membranes of Mycobacterium leprae and of cultivable Mycobacteria. Biol Cell 47:383–386.
14. Silva MT, Macedo PM. 1984. Ultrastructural characterization of normal and damaged membranes of Mycobacterium leprae and of cultivable mycobacteria. J Gen Microbiol 130:369–380. [PubMed]
15. Silva MT, Macedo PM. 1983. The interpretation of the ultrastructure of mycobacterial cells in transmission electron microscopy of ultrathin sections. Int J Lepr Other Mycobact Dis 51:225–234.
16. Paul TR, Beveridge TJ. 1992. Reevaluation of envelope profiles and cytoplasmic ultrastructure of mycobacteria processed by conventional embedding and freeze-substitution protocols. J Bacteriol 174:6508–6517 http://dx.doi.org/10.1128/jb.174.20.6508-6517.1992. [PubMed]
17. Paul TR, Beveridge TJ. 1994. Preservation of surface lipids and determination of ultrastructure of Mycobacterium kansasii by freeze-substitution. Infect Immun 62:1542–1550.
18. Hoffmann C, Leis A, Niederweis M, Plitzko JM, Engelhardt H. 2008. Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc Natl Acad Sci USA 105:3963–3967 http://dx.doi.org/10.1073/pnas.0709530105. [PubMed]
19. Sani M, Houben ENG, Geurtsen J, Pierson J, de Punder K, van Zon M, Wever B, Piersma SR, Jiménez CR, Daffé M, Appelmelk BJ, Bitter W, van der Wel N, Peters PJ. 2010. Direct visualization by cryo-EM of the mycobacterial capsular layer: a labile structure containing ESX-1-secreted proteins. PLoS Pathog 6:e1000794 http://dx.doi.org/10.1371/journal.ppat.1000794. [PubMed]
20. Jarlier V, Nikaido H. 1990. Permeability barrier to hydrophilic solutes in Mycobacterium chelonei. J Bacteriol 172:1418–1423 http://dx.doi.org/10.1128/jb.172.3.1418-1423.1990. [PubMed]
21. Niederweis M, Danilchanka O, Huff J, Hoffmann C, Engelhardt H. 2010. Mycobacterial outer membranes: in search of proteins. Trends Microbiol 18:109–116 http://dx.doi.org/10.1016/j.tim.2009.12.005. [PubMed]
22. Chapman GB, Hanks JH, Wallace JH. 1959. An electron microscope study of the disposition and fine structure of Mycobacterium lepraemurium in mouse spleen. J Bacteriol 77:205–211.
23. Hanks JH. 1961. The problem of preserving internal structures in pathogenic mycobacteria by conventional methods of fixation. Int J Lepr 29:175–178.
24. Hanks JH. 1961c. Demonstration of capsules on M. leprae during carbol-fuchsin staining mechanism of the Ziehl-Neelsen stain. Int J Lepr 26:179–182.
25. Hanks JH, Moore JT, Michaels JE. 1961. Significance of capsular components of Mycobacterium leprae and other mycobacteria. Int J Lepr 29:74–83.
26. Hanks JH. 1961. Capsules in electron micrographs of Mycobacterium leprae. Int J Lepr 29:84–87.
27. Fréhel C, Ryter A, Rastogi N, David H. 1986. The electron-transparent zone in phagocytized Mycobacterium avium and other mycobacteria: formation, persistence and role in bacterial survival. Ann Inst Pasteur Microbiol 137B:239–257 http://dx.doi.org/10.1016/S0769-2609(86)80115-6.
28. Ryter A, Fréhel C, Rastogi N, David HL. 1984. Macrophage interaction with mycobacteria including M. leprae. Acta Leprol 2:211–226.
29. Daffé M, Etienne G. 1999. The capsule of Mycobacterium tuberculosis and its implications for pathogenicity. Tuber Lung Dis 79:153–169 http://dx.doi.org/10.1054/tuld.1998.0200. [PubMed]
30. Fréhel C, Rastogi N, Bénichou JC, Ryter A. 1988. Do test tube-grown pathogenic mycobacteria possess a protective capsule? FEMS Microbiol Lett 56:225–230 http://dx.doi.org/10.1111/j.1574-6968.1988.tb03182.x.
31. Chiaradia L, Lefebvre C, Parra J, Marcoux J, Burlet-Schiltz O, Etienne G, Tropis M, Daffé M. 2017. Dissecting the mycobacterial cell envelope and defining the composition of the native mycomembrane. Sci Rep 7:12807 http://dx.doi.org/10.1038/s41598-017-12718-4. [PubMed]
32. Rezwan M, Lanéelle MA, Sander P, Daffé M. 2007. Breaking down the wall: fractionation of mycobacteria. J Microbiol Methods 68:32–39 http://dx.doi.org/10.1016/j.mimet.2006.05.016. [PubMed]
33. Minnikin DE. 1982. Lipids: complex lipids, their chemistry, biosynthesis and roles, p 95–184. In Ratledge C, Stanford J (ed), The Biology of the Mycobacteria, vol. 1. Physiology, Identification and Classification. Academic Press, London, UK.
34. Ortalo-Magné A, Lemassu A, Lanéelle MA, Bardou F, Silve G, Gounon P, Marchal G, Daffé M. 1996. Identification of the surface-exposed lipids on the cell envelopes of Mycobacterium tuberculosis and other mycobacterial species. J Bacteriol 178:456–461 http://dx.doi.org/10.1128/jb.178.2.456-461.1996. [PubMed]
35. Dhiman RK, Dinadayala P, Ryan GJ, Lenaerts AJ, Schenkel AR, Crick DC. 2011. Lipoarabinomannan localization and abundance during growth of Mycobacterium smegmatis. J Bacteriol 193:5802–5809 http://dx.doi.org/10.1128/JB.05299-11. [PubMed]
36. Bansal-Mutalik R, Nikaido H. 2014. Mycobacterial outer membrane is a lipid bilayer and the inner membrane is unusually rich in diacyl phosphatidylinositol dimannosides. Proc Natl Acad Sci USA 111:4958–4963 http://dx.doi.org/10.1073/pnas.1403078111. [PubMed]
37. Kaur D, Guerin ME, Skovierová H, Brennan PJ, Jackson M. 2009. Chapter 2: biogenesis of the cell wall and other glycoconjugates of Mycobacterium tuberculosis. Adv Appl Microbiol 69:23–78 http://dx.doi.org/10.1016/S0065-2164(09)69002-X.
38. Abrahams KA, Besra GS. 2016. Mycobacterial cell wall biosynthesis: a multifaceted antibiotic target. Parasitology 145:116–133. [PubMed]
39. Kotani S, Kitaura T, Hirano T, Tanaka A. 1959. Isolation and chemical composition of the cells walls of BCG. Biken’s J 2:129–141.
40. Draper P. 1971. The walls of Mycobacterium lepraemurium: chemistry and ultrastructure. J Gen Microbiol 69:313–324 http://dx.doi.org/10.1099/00221287-69-3-313. [PubMed]
41. Puech V, Chami M, Lemassu A, Lanéelle MA, 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 http://dx.doi.org/10.1099/00221287-147-5-1365. [PubMed]
42. Daffé M, Brennan PJ, 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.
43. Daffé M, McNeil M, Brennan PJ. 1993. Major structural features of the cell wall arabinogalactans of Mycobacterium, Rhodococcus, and Nocardia spp. Carbohydr Res 249:383–398 http://dx.doi.org/10.1016/0008-6215(93)84102-C.
44. McNeil M, Daffé M, Brennan PJ. 1990. Evidence for the nature of the link between the arabinogalactan and peptidoglycan of mycobacterial cell walls. J Biol Chem 265:18200–18206.
45. McNeil M, Daffé M, Brennan PJ. 1991. Location of the mycolyl ester substituents in the cell walls of mycobacteria. J Biol Chem 266:13217–13223.
46. Bhamidi S, Scherman MS, Jones V, Crick DC, Belisle JT, Brennan PJ, McNeil MR. 2011. Detailed structural and quantitative analysis reveals the spatial organization of the cell walls of in vivo grown Mycobacterium leprae and in vitro grown Mycobacterium tuberculosis. J Biol Chem 286:23168–23177 http://dx.doi.org/10.1074/jbc.M110.210534. [PubMed]
47. Barksdale L, Kim KS. 1977. Mycobacterium. Bacteriol Rev 41:217–372.
48. Benedetti EL, Dunia I, Ludosky MA, Nguyen VM, Dang DT, Rastogi N, David HL. 1984. Freeze-etching and freeze-fracture structural features of cell envelopes in mycobacteria and leprosy derived corynebacteria. Acta Leprol 2:237–248.
49. Chami M, Bayan N, Dedieu J, Leblon G, Shechter E, Gulik-Krzywicki T. 1995. Organization of the outer layers of the cell envelope of Corynebacterium glutamicum: a combined freeze-etch electron microscopy and biochemical study. Biol Cell 83:219–229 http://dx.doi.org/10.1016/0248-4900(96)81311-6.
50. Nguyen HT, Trach DD, Man NV, Ngoan TH, Dunia I, Ludosky-Diawara MA, Benedetti EL. 1979. Comparative ultrastructure of Mycobacterium leprae and Mycobacterium lepraemurium cell envelopes. J Bacteriol 138:552–558.
51. Rulong S, Aguas AP, da Silva PP, Silva MT. 1991. Intramacrophagic Mycobacterium avium bacilli are coated by a multiple lamellar structure: freeze fracture analysis of infected mouse liver. Infect Immun 59:3895–3902.
52. Draper P. 1998. The outer parts of the mycobacterial envelope as permeability barriers. Front Biosci 3:D1253–D1261 http://dx.doi.org/10.2741/A360.
53. Nikaido H, Kim SH, Rosenberg EY. 1993. Physical organization of lipids in the cell wall of Mycobacterium chelonae. Mol Microbiol 8:1025–1030 http://dx.doi.org/10.1111/j.1365-2958.1993.tb01647.x. [PubMed]
54. Villeneuve M, Kawai M, Kanashima H, Watanabe M, Minnikin DE, Nakahara H. 2005. Temperature dependence of the Langmuir monolayer packing of mycolic acids from Mycobacterium tuberculosis. Biochim Biophys Acta 1715:71–80 http://dx.doi.org/10.1016/j.bbamem.2005.07.005. [PubMed]
55. Villeneuve M, Kawai M, Watanabe M, Aoyagi Y, Hitotsuyanagi Y, Takeya K, Gouda H, Hirono S, Minnikin DE, Nakahara H. 2007. Conformational behavior of oxygenated mycobacterial mycolic acids from Mycobacterium bovis BCG. Biochim Biophys Acta 1768:1717–1726 http://dx.doi.org/10.1016/j.bbamem.2007.04.003. [PubMed]
56. Trias J, Benz R. 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 268:6234–6240.
57. Trias J, Jarlier V, Benz R. 1992. Porins in the cell wall of mycobacteria. Science 258:1479–1481 http://dx.doi.org/10.1126/science.1279810. [PubMed]
58. Senaratne RH, Mobasheri H, Papavinasasundaram KG, Jenner P, Lea EJ, Draper P. 1998. Expression of a gene for a porin-like protein of the OmpA family from Mycobacterium tuberculosis H37Rv. J Bacteriol 180:3541–3547.
59. Raynaud C, Papavinasasundaram KG, Speight RA, Springer B, Sander P, Böttger EC, Colston MJ, Draper P. 2002. The functions of OmpATb, a pore-forming protein of Mycobacterium tuberculosis. Mol Microbiol 46:191–201. http://dx.doi.org/10.1046/j.1365-2958.2002.03152.x. [PubMed]
60. Teriete P, Yao Y, Kolodzik A, Yu J, Song H, Niederweis M, Marassi FM. 2010. Mycobacterium tuberculosis Rv0899 adopts a mixed alpha/beta-structure and does not form a transmembrane beta-barrel. Biochemistry 49:2768–2777. http://dx.doi.org/10.1021/bi100158s. [PubMed]
61. Faller M, Niederweis M, Schulz GE. 2004. The structure of a mycobacterial outer-membrane channel. Science 303:1189–1192 http://dx.doi.org/10.1126/science.1094114. [PubMed]
62. Hartmann M, Barsch A, Niehaus K, Pühler A, Tauch A, Kalinowski J. 2004. The glycosylated cell surface protein Rpf2, containing a resuscitation-promoting factor motif, is involved in intercellular communication of Corynebacterium glutamicum. Arch Microbiol 182:299–312 http://dx.doi.org/10.1007/s00203-004-0713-1. [PubMed]
63. Danilchanka O, Pires D, Anes E, Niederweis M. 2015. The Mycobacterium tuberculosis outer membrane channel protein CpnT confers susceptibility to toxic molecules. Antimicrob Agents Chemother 59:2328–2336. [PubMed]
64. Speer A, Sun J, Danilchanka O, Meikle V, Rowland JL, Walter K, Buck BR, Pavlenok M, Hölscher C, Ehrt S, Niederweis M. 2015. Surface hydrolysis of sphingomyelin by the outer membrane protein Rv0888 supports replication of Mycobacterium tuberculosis in macrophages. Mol Microbiol 97:881–897 http://dx.doi.org/10.1111/mmi.13073. [PubMed]
65. Boddingius J, Dijkman H. 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 136:2001–2012 http://dx.doi.org/10.1099/00221287-136-10-2001. [PubMed]
66. Hunter SW, Brennan PJ. 1990. Evidence for the presence of a phosphatidylinositol anchor on the lipoarabinomannan and lipomannan of Mycobacterium tuberculosis. J Biol Chem 265:9272–9279.
67. Rastogi N, Lévy-Frebault V, Blom-Potar MC, David HL. 1989. Ability of smooth and rough variants of Mycobacterium avium and M. intracellulare to multiply and survive intracellularly: role of C-mycosides. Zentralbl Bakteriol Mikrobiol Hyg A 270:345–360 http://dx.doi.org/10.1016/S0176-6724(89)80003-3.
68. Daffé M, Lacave C, Lanéelle MA, Lanéelle G. 1987. Structure of the major triglycosyl phenol-phthiocerol of Mycobacterium tuberculosis (strain Canetti). Eur J Biochem 167:155–160 http://dx.doi.org/10.1111/j.1432-1033.1987.tb13317.x. [PubMed]
69. Lemassu A, Ortalo-Magné A, Bardou F, Silve G, Laneélle MA, Daffé M. 1996. Extracellular and surface-exposed polysaccharides of non-tuberculous mycobacteria. Microbiology 142:1513–1520 http://dx.doi.org/10.1099/13500872-142-6-1513. [PubMed]
70. Ortalo-Magné A, Dupont MA, Lemassu A, Andersen ÅB, Gounon P, Daffé M. 1995. Molecular composition of the outermost capsular material of the tubercle bacillus. Microbiology 141:1609–1620 http://dx.doi.org/10.1099/13500872-141-7-1609. [PubMed]
71. Lemassu A, Daffé M. 1994. Structural features of the exocellular polysaccharides of Mycobacterium tuberculosis. Biochem J 297:351–357 http://dx.doi.org/10.1042/bj2970351. [PubMed]
72. Raynaud C, Etienne G, Peyron P, Lanéelle MA, Daffé M. 1998. Extracellular enzyme activities potentially involved in the pathogenicity of Mycobacterium tuberculosis. Microbiology 144:577–587 http://dx.doi.org/10.1099/00221287-144-2-577. [PubMed]
73. Dinadayala P, Lemassu A, Granovski P, Cérantola S, Winter N, Daffé M. 2004. Revisiting the structure of the anti-neoplastic glucans of Mycobacterium bovis Bacille Calmette-Guerin. Structural analysis of the extracellular and boiling water extract-derived glucans of the vaccine substrains. J Biol Chem 279:12369–12378 http://dx.doi.org/10.1074/jbc.M308908200. [PubMed]
74. Schwebach JR, Glatman-Freedman A, Gunther-Cummins L, Dai Z, Robbins JB, Schneerson R, Casadevall A. 2002. Glucan is a component of the Mycobacterium tuberculosis surface that is expressed in vitro and in vivo. Infect Immun 70:2566–2575. http://dx.doi.org/10.1128/IAI.70.5.2566-2575.2002. [PubMed]
75. Sonnenberg MG, Belisle JT. 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 65:4515–4524.
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2019-07-05
2019-11-13

Abstract:

The mycobacterial cell envelope consists of a typical plasma membrane of lipid and protein surrounded by a complex cell wall composed of carbohydrate and lipid. In pathogenic species, such as , an outermost “capsule” layer surrounds the cell wall. This wall embraces a fundamental, covalently linked “cell-wall skeleton” composed of peptidoglycan, solidly attached to arabinogalactan, whose penta-saccharide termini are esterified by very-long-chain fatty acids (mycolic acids). These fatty acids form the inner leaflet of an outer membrane, called the mycomembrane, whose outer leaflet consists of a great variety of non-covalently linked lipids and glycolipids. The thickness of the mycomembrane, which is similar to that of the plasma membrane, is surprising in view of the length of mycoloyl residues, suggesting dedicated conformations of these fatty acids. Finally, a periplasmic space also exists in mycobacteria, between the plasma membrane and the peptidoglycan. This article provides a comprehensive overview of this biologically important and structurally unique mycobacterial cell compartment.

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Image of FIGURE 1
FIGURE 1

Diagrams (adapted from references 11 and 17 19 ) of the cell envelopes extracted from images obtained by TEM, CEMOVIS of various bacterial cells, and cryoEM of whole-mount mycobacteria. AG, arabinogalactan; CEMOVIS, cryo-electron microscopy of vitreous sections; cryo-EM, cryo-electron microscopy; EDL, electron-dense layer; ETL, electron-transparent layer; FP, fracture plane; GL, granular layer; OL, outer layer; OM, outer membrane; PG, peptidoglycan; PM, plasma membrane; peri, periplasm; TEM, transmission electron microscopy.

Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0027-2018
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Image of FIGURE 2
FIGURE 2

Chemical structures of representative mycobacterial lipids and their export systems through the plasma membrane to reach their final locations in the outer membrane (mycomembrane) or/and capsular compartment of the cell envelope. Some of the lipids are ubiquitous (e.g., TMM and trehalose dimycolate), whereas other are species- or type species-specific (e.g., PAT, phthiocerol dimycocerosate, PGL-tb), found in selective mycobacterial species or strains. TMM is used to transfer its mycoloyl residue onto both the arabinan termini of AG and TMM to yield the cell wall skeleton mAGP and trehalose dimycolate, respectively. AcSGL, diacylated sulfoglycolipid; AG, arabinogalactan; DAT, diacyl trehalose; mAGP, mycoloyl-AG-peptidoglycan; mAGP, mycoloyl-AG-peptidoglycan; MmpL, mycobacterial membrane protein large; PAT, polyacyltrehalose; PDIM, phthiocerol dimycocerosate; PGL-tb, phenol glycolipid of ; SL-I, sulfolipid I, the major sulfolipid of ; TDM, trehalose dimycolate; TMM, trehalose monomycolate.

Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0027-2018
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Image of FIGURE 3
FIGURE 3

Model of the mycobacterial cell envelope. The cell envelope consists of a plasma membrane, a periplasm, the cell wall skeleton, and the outermost layer, called capsule in the case of pathogenic species. The plasma membrane is composed of phospholipids (e.g., PIM), lipopolysaccharides (e.g., LAM), and proteins, which include MmpL involved in the transport of lipids. The periplasmic space contains the GL and, presumably other proteins. The cell wall skeleton is made of peptidoglycan, arabinogalactan and mycolic acid residues that form the inner leaflet of the outer membrane (mycomembrane). The outer leaflet of the latter membrane is composed of various lipids, notably, trehalose mycolates. The capsular layer is a matrix of glucan that contains proteins, (lipo)polysaccharides, and small amounts of lipids. AM, arabinomannan; LAM, lipoAM; GL, granular layer; MmpL, mycobacterial membrane protein large; PIM, phosphatidyl inositol mannosides; PL, phospholipids; TDM, trehalose dimycolate; TMM, trehalose monomycolate.

Source: microbiolspec July 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.GPP3-0027-2018
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