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Review
. 2019 Jul;7(4):10.1128/microbiolspec.gpp3-0027-2018.
doi: 10.1128/microbiolspec.GPP3-0027-2018.

Unraveling the Structure of the Mycobacterial Envelope

Mamadou Daffé  1 , Hedia Marrakchi  1
Affiliations
Review

Unraveling the Structure of the Mycobacterial Envelope

Mamadou Daffé et al. Microbiol Spectr. 2019 Jul.

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 Mycobacterium tuberculosis, 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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Figures

FIGURE 1
FIGURE 1
Diagrams (adapted from references and –19) of the cell envelopes extracted from images obtained by (A) TEM, (B) CEMOVIS of various bacterial cells, and (C) 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.
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. Ac2SGL, 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 M. tuberculosis; SL-I, sulfolipid I, the major sulfolipid of M. tuberculosis; TDM, trehalose dimycolate; TMM, trehalose monomycolate.
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.
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