Skip to main content
SpringerLink
Log in

Cell envelope composition and organisation in the genus Rhodococcus

  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

A knowledge of the organisation of the rhodococcal cell envelope is of fundamental importance if the environmental and biotechnological significance of these bacteria are to be understood and succesfully exploited. The genus Rhodococcus belongs to a distinctive suprageneric taxon, the mycolata, which includes among others the genera Corynebacterium, Mycobacterium and Nocardia. Members of this taxon exhibit an unusual complexity in their cell envelope composition and organisation compared to other Gram-positive bacteria. Models that describe the architecture of the mycobacterial cell envelope are extrapolated here to provide a model of the rhodococcal cell envelope. The rhodococcal cell envelope is dominated by the presence of an arabinogalactan cell wall polysaccharide and large 2-alkyl 3-hydroxy branched-chain fatty acids, the mycolic acids, which are covalently assembled into a peptidoglycan–arabinogalactan–mycolic acid matrix. This review further emphasises that the mycolic acids in this complex form the basis of an outer lipid permeability barrier. The localisation and roles of other cell envelope components, notably complex free lipids, lipoglycans, proteins and lipoproteins are also considered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alshamaony L, Goodfellow M & Minnikin DE (1976) Free mycolic acids as criteria in the classification of Nocardia and the & #x2019;rhodochrous & #x2019; complex. J. Gen. Microbiol. 92: 188–199

    Google Scholar 

  • Alvarez HM, Mayer F, Fabritius D & Steinb & #x00FC;chel A (1996) Formation of intracytoplasmic lipid inclusions by Rhodococcus opacus strain PD630. Arch. Microbiol. 165: 377–386

    Google Scholar 

  • Asselineau C & Asselineau J (1978) Trehalose-containing glycolipids. Progr. Chem. Fats other Lipids 16: 59–99

    Google Scholar 

  • Atrat PG, Wagner B, Wagner M & Schumann G (1992) Localization of the cholesterol oxidase in Rhodococcus erythropolis IMET 7185 studied by immunoelectron microscopy. J. Steroid Biochem. Molec. Biol. 42: 193–200

    Google Scholar 

  • Barry CE & Mdluli K (1996) Drug sensitivity and environmental adaption of mycobacterial cell wall components. Trends Microbiol. 4: 275–281

    Google Scholar 

  • Barton MD, Goodfellow M & Minnikin DE (1989) Lipid composition in the classification of Rhodococcus equi. Zbl. Bakteriol. 272: 154–170

    Google Scholar 

  • Belisle JT, Vissa VD, Sievert T, Takayama K, Brennan PJ & Besra GS (1997) Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis. Science 276: 1420–1422

    Google Scholar 

  • Bendinger B, Rijnaarts HHM, Altendorf K & Zehnder AJB (1993) Physicochemical cell surface and adhesive properties of coryneform bacteria related to the presence of and chain length of mycolic acids. Appl. Env. Microbiol. 59: 3973–3977

    Google Scholar 

  • Besra GS, Khoo K-H, McNeil MR, Dell A, Morris HR & Brennan PJ (1995) A new interpretation of the structure of the mycolyl-arabinogalactan complex of Mycobacterium tuberculosis as revealed through characterization of oligoglycosylalditol fragments by fast-atom bombardment mass spectrometry and 1H nuclear magnetic resonance spectroscopy. Biochemistry 34: 4257–4266

    Google Scholar 

  • Brennan PJ & Nikaido H (1995) The envelope of mycobacteria. Ann. Rev. Biochem. 64: 29–63

    Google Scholar 

  • Briglia M, Rainey FA, Stackebrandt E, Schraa G & Salkinoja-Salonen MS (1996) Rhodococcus percolatus sp. nov., a bacterium degrading 2,4,6-trichlorophenol. Int. J. Syst. Bacteriol. 46: 23–30

    Google Scholar 

  • Chun J, Kang S-O, Hah YC & Goodfellow M (1996) Phylogeny of mycolic acid-containing actinomycetes. J. Ind. Microbiol. 17: 205–213

    Google Scholar 

  • Chun J, Blackall LL, Kang S-O, Hah YC & Goodfellow M(1997) A proposal to reclassify Nocardia pinensis Blackall et al. as Skermania piniformis gen. nov., comb. nov. Int. J. Syst. Bacteriol. 47: 127–131

    Google Scholar 

  • Daffe M & Draper P (1998) The envelope layers of mycobacteria with reference to their pathogenicity. Adv. Microb. Physiol. 39: 131–203

    Google Scholar 

  • Daffe 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

    Google Scholar 

  • de Almeida ET & Ioneda T (1989) Composition and toxicity of lipids from Rhodococcus rhodochrous grown on medium containing galactose, glucose or mannose. Biochim. Biophys. Acta 1005: 45–50

    Google Scholar 

  • Delmas C, Gilleron M, Brando T, Vercellone A, Gheorghiu M, Riviere M & Puzo G (1997) Comparative structural analysis of the mannosylated-lipoarabinomannans from Mycobacterium bovis BCG vaccine strains: characterisation and localisation of succinates. Glycobiology 7: 811–817

    Google Scholar 

  • Dufrêne YF, van der Wal A, Norde W & Rouxhet PG (1997) X-ray photoelectron spectroscopy analysis of whole cells and isolated cell walls of Gram-positive bacteria: comparison with biochemical analysis. J. Bacteriol. 179: 1023–1028

    Google Scholar 

  • Durand E, Welby M, Lan & #x00E9;elle G & Tocanne J-F (1979) Phase behaviour of cord factor and related bacterial glycolipid toxins. A monolayer study. Eur. J. Biochem. 93: 103–112

    Google Scholar 

  • Fischer W (1994) Lipoteichoic acids and lipoglycans. In: (Ghuysen J-M & Hakenbeck R (Eds) New Comprehensive Biochemistry, Vol. 27, Bacterial Cell Wall (pp 199–215). Elsevier Science, Amsterdam

    Google Scholar 

  • Flaherty C, Minnikin DE & Sutcliffe IC (1996) A chemotaxonomic study of the lipoglycans of Rhodococcus rhodnii N445 (NCIMB 11279). Zbl. Bakteriol. 285: 11–19

    Google Scholar 

  • Fujioka M, Koda S & Morimoto Y (1985) Novel glycosidic linkage between arabinogalactan and peptidoglycan in the cell wall skeleton of Nocardia rubra AN-115. J. Gen. Microbiol. 131: 1323–1329

    Google Scholar 

  • Garrison RG, Mirikitani FK & Lane JW (1983) Fine structural studies of Rhodococcus species. Microbios 36: 183–190

    Google Scholar 

  • Goodfellow M (1992) The family Nocardiaceae. In: Balows A, Trüper HG, Dworkin M, Harder W & Schleifer K-H (Eds) The Prokaryotes (pp 1188–1213). Springer-Verlag, New York

    Google Scholar 

  • Hunter SW, Gaylord H & Brennan PJ (1986) Structure and antigenicity of the phosphorylated lipopolysaccharide antigens from the leprosy and tubercle bacilli. J. Biol. Chem. 261: 12345–12351

    Google Scholar 

  • Ioneda T & Ono SS (1996) Chromatographic and mass spectrometric analyses of 1-monomycolyl glycerol fraction from Rhodococcus lentifragmentus as per-O-benzoyl derivatives. Chem. Phys. Lipids 81: 11–19

    Google Scholar 

  • Khoo K-H, Dell A, Morris HR, Brennan PJ & Chatterjee D (1995) Structural definition of acylated phosphatidylinositol mannosides from Mycobacterium tuberculosis: definition of a common anchor for lipomannan and lipoarabinomannan. Glycobiology 5: 117–127.

    Google Scholar 

  • Klatte S, Kroppenstedt RM & Rainey FA (1994) Rhodococcus opacus sp. nov., an unusual nutritionally versatile Rhodococcus species. Syst. Appl. Microbiol. 17: 355–360

    Google Scholar 

  • Koronelli TV (1988) Investigation of the lipids of saprophytic mycobacteria in the U.S.S.R. J. Chromatog. 440: 479–486

    Google Scholar 

  • Kretschmer A, Bock H & Wagner F (1982) Chemical and physical characterisation of interfacial-active lipids from Rhodococcus erythropolis grown on n-alkanes. Appl. Env. Microbiol. 44: 864–870

    Google Scholar 

  • Kurane R, Hatamochi K, Kakuno T, Kiyohara M, Tajima T, Hirano M & Taniguchi Y (1995) Chemical structure of lipid bioflocculant produced by Rhodococcus erythropolis. Biosci. Biotech. Biochem. 59: 1652–1656

    Google Scholar 

  • Lang S & Philp J (1998) Surface-active lipids in rhodococci. Antonie van Leeuwenhoek 74: 59–70

    Google Scholar 

  • Matsunaga I, Oka S, Fujiwara N & Yano I (1996) Relationship between induction of macrophage chemotactic factors and formation of granulomas caused by mycolyl glycolipids from Rhodococcus ruber (Nocardia rubra). J. Biochem. 120: 663–670

    Google Scholar 

  • Minnikin D E (1982) Lipids: Complex lipids, their chemistry, biosynthesis and roles. In: Ratledge C & Stanford JL (Eds) The Biology of the Mycobacteria (pp 95–184). Academic Press, London

    Google Scholar 

  • Minnikin DE (1991) Chemical principles in the organization of lipid components in the mycobacterial cell envelope. Res. Microbiol. 142: 423–427

    Google Scholar 

  • Minnikin D E & O & #x2019;Donnell A G (1984) Actinomycete envelope lipid and peptidoglycan composition. In: Goodfellow M, Mordarski M & Williams ST (Eds) The Biology of the Actinomycetes (pp 337–388). Academic Press, London

    Google Scholar 

  • Moormann M, Z & #x00E4;hringer U, Moll H, Kaufmann R, Schmid R & Altendorf K (1997) A new glycosylated lipopeptide incorporated into the cell wall of a smooth variant of Gordona hydrophobica. J. Biol. Chem. 272: 10729–10738

    Google Scholar 

  • Mukhopadhyay S, Basu D & Chakrabarti P (1997) Characterization of a porin from Mycobacterium smegmatis. J. Bacteriol. 179: 6205–6207

    Google Scholar 

  • Niederweis M, Maier E, Lichtinger T, Benz R & Kr & #x00E4;mer R (1995) Identification of channel-forming activity in the cell wall of Corynebacterium glutamicum J. Bacteriol. 177: 5716–5718

    Google Scholar 

  • Nigou J, Gilleron M, Cahuzac B, Boun & #x00E9;ry J-D, Herold M, Thurnher M & Puzo G (1997) The phosphatidyl-myo-inositol anchor of the lipoarabinomannans from Mycobacterium bovis Bacillus Calmette Gu & #x00E9;rin. Heterogeneity, structure and role in the regulation of cytokine secretion. J. Biol. Chem. 272: 23094–23103

    Google Scholar 

  • Powalla M, Lang S & Wray V (1989) Penta-and disaccharide lipid formation by Nocardia corynebacteroides grown on n-alkanes. Appl. Microbiol. Biotechnol. 31: 473–479

    Google Scholar 

  • Rainey FA, Burghardt J, Kroppenstedt RM, Klatte S & Stackebrandt E (1995) Phylogenetic analysis of the genera Rhodococcus and Nocardia and evidence for the evolutionary origin of the genus Nocardia from within the radiation of Rhodococcus species. Microbiology 141: 523–528

    Google Scholar 

  • Stephens GM & Dalton H (1987) Is toxin production by coryneform bacteria linked to their ability to utilize hydrocarbons? Trends Biotechnol. 5: 5–7

    Google Scholar 

  • Sunairi M, Iwabuchi N, Yoshizawa Y, Murooka H, Morisaki H & Nakajima M (1997) Cell-surface hydrophobicity and scum formation of Rhodococcus rhodochrous strains with different colonial morphologies. J. Appl. Bacteriol. 82: 204–210

    Google Scholar 

  • Sutcliffe IC (1994) The lipoteichoic acids and lipoglycans of Grampositive bacteria: a chemotaxonomic perspective. Syst. Appl. Microbiol. 17: 467–480

    Google Scholar 

  • Sutcliffe IC (1995) Identification of a lipoarabinomannan-like lipoglycan in Corynebacterium matruchotii. Arch. Oral Biol. 40: 1119–1124

    Google Scholar 

  • Sutcliffe IC (1997) Macroamphiphilic cell envelope components of Rhodococcus equi and closely related bacteria. Vet. Microbiol. 56: 287–299

    Google Scholar 

  • Sutcliffe IC & Alderson G (1995) A chemotaxonomic appraisal of the distribution of lipomannans within the genus Micrococcus. FEMS Microbiol. Letts. 133: 233–237

    Google Scholar 

  • Sutcliffe IC & Russell RRB (1995) Lipoproteins of Gram-positive bacteria. J. Bacteriol. 177: 1123–1128

    Google Scholar 

  • Takai S, Iie M, Watanabe Y, Tsubaki S & Sekizaki T (1992) Virulence-associated 15-to 17-kilodalton antigens in Rhodococcus equi: temperature-dependent expression and location of the antigens. Infect. Immun. 60: 2995–2997

    Google Scholar 

  • Takaichi S, Tamura Y, Azegami K, Yamamoto Y & Ishidsu J-I (1997) Carotenoid glucoside mycolic acid esters from the nocardioform actinomycetes, Rhodococcus rhodochrous. Phytochem. 45: 505–508

    Google Scholar 

  • Tan C, Prescott JF, Patterson MC & Nicholson VM (1995) Molecular characterization of a lipid-modified virulence-associated protein of Rhodococcus equi and its potential in protective immunity. Can. J. Vet. Res. 59: 51–59

    Google Scholar 

  • Tomiyasu I, Toriyama S, Yano I & Masui M (1981) Changes in molecular species composition of nocardomycolic acids in Nocardia rubra by the growth temperature. Chem. Phys. Lipids 28: 41–54

    Google Scholar 

  • Tomiyasu I & Yano I (1984) Isonicotinic acid hydrazide induced changes and inhibition in mycolic acid synthesis in Nocardia and related taxa. Arch. Microbiol. 137: 316–323

    Google Scholar 

  • Trias J, Jarlier V & Benz R (1992) Porins in the cell wall of mycobacteria. Science 258: 1479–1481

    Google Scholar 

  • Uchida K & Aida K (1979) Taxonomic significance of cell-wall acyl type in Corynebacterium–Mycobacterium–Nocardia group by a glycolate test. J. Gen. Appl. Microbiol. 25: 169–183

    Google Scholar 

  • Uchida Y, Tsuchiya R, Chino M, Hirano J & Tabuchi T (1989) Extracellular accumulation of mono-and di-succinoyl trehalose lipids by a strain of Rhodococcus erythropolis grown on n-alkanes. Agric. Biol. Chem. 53: 757–763

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Fleming Building, School of Health Sciences, The University of Sunderland, Sunderland, SR2 3SD, UK

    Iain C. Sutcliffe

Authors
  1. Iain C. Sutcliffe
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sutcliffe, I.C. Cell envelope composition and organisation in the genus Rhodococcus. Antonie Van Leeuwenhoek 74, 49–58 (1998). https://doi.org/10.1023/A:1001747726820

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1001747726820

Search

Navigation