Glycoprotein Nature of Select Bacterial S-Layers

  • Paul Messner
  • Judith Schuster - Kolbe
  • Christina Schäffer
  • Uwe B. Sleytr
  • Rudolf Christian
Part of the NATO ASI Series book series (NSSA, volume 252)


Nowadays it is established knowledge that procaryotes are able to synthesize true glycoproteins. The first proven reports on bacterial glycoproteins reach back into the mid — 1970s when Mescher and Strominger (1976) published a partial structure of the glycan chains from the surface layer glycoprotein of the halophilic archaeobacterium Halobacterium (halobium) salinarium. According to the recently introduced taxonomic terminology we use in this article the terms archaea and bacteria instead of archaeobacteria and eubacteria (Woese et al., 1990). With the rapid ongoing research on archaea it soon became obvious that most of these procaryotes are covered by glycosylated surface layer (S-layer) glycoproteins (for reviews see Kandier, 1982; Kandier and König, 1985; König and Stetter, 1986; Sumper, 1987; König, 1988a; Lechner and Wieland, 1989). On the other hand, it was widely believed that bacteria (eubacteria) were not able to glycosylate proteins even though Sleytr and Thorne (1976) had provided early evidence for the occurrence of bacterial glycoproteins. For some time it was even considered that the surface glycosylation was a taxonomic criterion for the discrimination between archaea and bacteria (Mescher, 1981; Kandier, 1982).


Amino Sugar Clostridium Thermocellum Deinococcus Radiodurans Glycan Chain Trifluoromethane Sulfonic Acid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Altman, E., Brisson, J.-R., Messner, P., and Sleytr, U.B., 1990, Chemical characterization of the regularly arranged surface layer glycoprotein of Clostridium thermosaccharolyticum D120–70, Eur. J. Biochem. 188: 73.PubMedCrossRefGoogle Scholar
  2. Altman, E., Brisson, J.-R., Gagné, S.M., Kolbe, J., Messner, P., and Sleytr, U.B., 1992, Structure of the glycan chain from the surface layer glycoprotein of Clostridium thermohydrosulfuricum L77–66, Biochim. Biophys. Acta 1117: 71.PubMedCrossRefGoogle Scholar
  3. Buckmire, F.L.A., and Murray, R.G.E., 1973, Studies on the cell wall of Spirillum sevens. II. Chemical characterization of the outer structured layer, Can. J. Microbiol. 19: 59.PubMedCrossRefGoogle Scholar
  4. Christian, R., Messner, P., Weiner, C., Sleytr, U.B., and Schulz, G., 1988, Structure of a glycan from the surface-layer glycoprotein of Clostridium thermohydrosulfuricum strain L111–69, Carbohyd. Res. 176: 160.CrossRefGoogle Scholar
  5. Cleveland, D.W., Fischer, S.G., Kirschner, M.W., and Laemmli, U.K., 1977, Peptide mapping by limited proteolysis in sodium dodecyl sulphate and analysis by gel electrophoresis, J. Biol. Chem. 252: 1102.PubMedGoogle Scholar
  6. Creighten, T.E., 1979, Electrophoretic analysis of the unfolding of proteins by urea, J. Mol. Biol. 129: 235.CrossRefGoogle Scholar
  7. Edge, A.B.S., Faltynek, C.R., Hof, L, Reichert, Jr., L.E., and Weber, P., 1981, Deglycosylation of glycoproteins by trifluoromethanesulfonic acid, Anal. Biochem. 118: 131.PubMedCrossRefGoogle Scholar
  8. Garcia-Garibay, M., and Marshall, V.M.E., 1991, Polymer production by Lactobacillus delbrueckii subsp. bulgaricus, J. Appl. Bacteriol. 70: 325.CrossRefGoogle Scholar
  9. Gerwig, G.J., deWaard, P., Kamerling, J.P., Vliegenthart, J.F.G., Morgenstern, E., Lamed, R., and Bayer, E.A., 1989, Novel 0-linked carbohydrate chains in the cellulase complex (cellulosome) of Clostridium thermocellum, J. Biol. Chem. 264: 1027.PubMedGoogle Scholar
  10. Gerwig, G.J., Kamerling, J.P., Vliegenthart, J.F.G., Morag (Morgenstern), E., Lamed, R., and Bayer, E.A., 1991, Primary structure of 0-linked carbohydrate chains in the cellulosome of different Clostridium thermocellum strains, Eur. J. Biochem. 196: 115.Google Scholar
  11. Görg, A., Postel, W., Westermeier R., Gianazza, E., and Righetti, P.G., 1981, SDSgel gradient electrophoresis, isoelectric focusing and high-resolution two-dimensional electrophoresis in horizontal, ultrathin-layer polyacrylamide gels, in: “Electrophoresis ‘81”, R.C. Allen and P. Arnaud, eds., Walter de Gruyter, Berlin.Google Scholar
  12. Haselbeck, A., and Hösel, W., 1990, Description and application of an immunological detection system for analyzing glycoproteins on blots, Glycoconjugate J. 7: 63.CrossRefGoogle Scholar
  13. Hollaus, F., and Sleytr, U., 1972, On the taxonomy and fine structure of some hyperthermophilic saccharolytic clostridia, Arch. Microbiol. 86: 129.Google Scholar
  14. Kandler, O., 1982, Cell wall structures and their phylogenetic implications, Zbl. Bakt. Hyg., I. Abt. Orig. C 3: 149.Google Scholar
  15. Kandler, O., and König, H., 1985, Cell envelopes of archaebacteria, in: “The Bacteria”, Vol. VIII, “Archaebacteria”, C.R. Woese and R.S. Wolfe, eds., Academic Press, New York.Google Scholar
  16. Kawamura, T., and Shockman, G.D., 1983, Purification and some properties of the endogenous, autolytic N-acetylmuramoylhydrolase of Streptococcus faecium, a bacterial glycoenzyme, J. Biol. Chem. 258: 9514.PubMedGoogle Scholar
  17. König, H., 1988a, Archaeobacterial cell envelopes, Can. J. Microbiol. 34:395. König, H., 1988b, Archaeobacteria, in: “Biotechnology”, Vol. 6b, H.-J. Rehm, ed., VCH Publishers, Weinheim.Google Scholar
  18. König, H., and Stetter, KO., 1986, Studies on archaebacterial S-layers, System. Appl. Microbiol. 7: 300.CrossRefGoogle Scholar
  19. Koval, S.F., 1988, Paracrystalline protein surface arrays on bacteria, Can. J. Microbiol. 34: 407.CrossRefGoogle Scholar
  20. Küpcü, Z., März, L, Messner, P., and Sleytr, U.B., 1984, Evidence for the glycoprotein nature of the crystalline cell wall surface layer of Bacillus stearothermophilus strain NRS 2004/3a, FEBS Lett. 173: 185.PubMedCrossRefGoogle Scholar
  21. Lechner, J., and Wieland, F., 1989, Structure and biosynthesis of prokaryotic glycoproteins, Annu. Rev. Biochem. 58: 173.PubMedCrossRefGoogle Scholar
  22. Lewis, LO., Yousten, A.A., and Murray, R.G.E., 1987, Characterisation of the surface protein layers of the mosquito-pathogenic strains of Bacillus sphaericus, J. Bacteriol. 169: 72.PubMedGoogle Scholar
  23. Macura, D., and Townsley, P.M., 1984, Scandinavian ropy milk - identification and characterization of endogenous ropy lactic streptococci and their extracellular secretion, J. Dairy Sci. 67: 735.CrossRefGoogle Scholar
  24. Maeba, P.Y., 1986, Isolation of a surface glycoprotein from Myxococcus xanthus, J. Bacteriol. 166: 644.PubMedGoogle Scholar
  25. Malcolm, A.J., Messner, P., Sleytr, U.B., Smith, R.H., and Unger, F.M., 1993, Crystalline bacterial cell surface layers as combined carrier/adjuvants for conjugate vaccines, in: “Immobilised Macromolecules: Application Potentials”, U.B. Sleytr, P. Messner, D. Pum, and M. Sara, eds., Springer-Verlag, London.Google Scholar
  26. Matteuzzi, D., Hollaus, F., and Biavati, B., 1978, Proposal of neotype for Clostridium thermohydrosulfuricum and merging of Clostridium tartarivorum with Clostridium thermosaccharolyticum, Int. J. Syst. Bacteriol. 28: 528.CrossRefGoogle Scholar
  27. Mengele, R., and Sumper, M., 1992, Drastic differences in glycosylation of related Slayer glycoproteins from moderate and extreme halophiles, J. Biol. Chem. 267: 8182.PubMedGoogle Scholar
  28. Mescher, M.F., 1981, Glycoproteins as cell-surface structural components, Trends Biol. Sci. 6: 97.CrossRefGoogle Scholar
  29. Mescher, M.F., and Strominger, J.L, 1976, Purification and characterization of a prokaryotic glycoprotein from the cell envelope of Halobacterium salinarium, J. Biol. Chem. 251: 2005.Google Scholar
  30. Messner, P., and Sleytr, U.B., 1988a, Asparaginyl-rhamnose: a novel type of protein-carbohydrate linkage in a eubacterial surface-layer glycoprotein, FEBS Lett. 228: 317.PubMedCrossRefGoogle Scholar
  31. Messner, P., and Sleytr, U.B., 1988b, Separation and purification of S-layers from gram-positive and gram-negative bacteria, in: “Bacterial Cell Surface Techniques”, I.C. Hancock and I.R. Poxton, eds., John Wiley and Sons, Chichester.Google Scholar
  32. Messner, P., and Sleytr, U.B., 1991, Bacterial surface layer glycoproteins, Glycobiology 1: 545.PubMedCrossRefGoogle Scholar
  33. Messner, P., and Sleytr, U.B., 1992, Crystalline bacterial cell-surface layers, Adv. Microbial Physiol. 33: 213.CrossRefGoogle Scholar
  34. Messner, P., Küpcü, S., Sara, M., Pum, D., and Sleytr, U.B., 1991, Characterization and biotechnological application of eubacterial glycoproteins, in: “Protein Glycosylation: Cellular, Biotechnological and Analytical Aspects”, GBF Monographs, Vol. 15, H.S. Conradt, ed., VCH Verlagsgesellschaft, Weinheim.Google Scholar
  35. Messner, P., Christian,R., Kolbe, J., Schulz, G., and Sleytr, U.B., 1992a, Analysis of a novel linkage unit of 0-linked carbohydrates from the crystalline surface layer glycoprotein of Clostridium thermohydrosulfuricum S102–70, J. Bacteriol. 174: 2236.Google Scholar
  36. Messner, P., Mazid, M.A., Unger, F.M., and Sleytr, U.B., 1992b, Artificial antigens. Synthetic carbohydrate haptens immobilized on crystalline bacterial surface layer glycoproteins. Carbohydr. Res., 233: 175.PubMedCrossRefGoogle Scholar
  37. Muthukumar, G., and Nickerson, K.W., 1987, The glycoprotein toxin of Bacillus thuringiensis subsp. israelensis indicates a lectin-like receptor in the larval mosquito gut, Appl. Environ. Mirobiol. 53: 2650.Google Scholar
  38. Peters, J., Peters, M., Lottspeich, F., Schäfer, W., and Baumeister, W., 1987, Nucleotide sequence analysis of the gene encoding the Deinococcus radiodurans surface protein, derived amino acid sequence and complementary protein chemical studies, J. Bacteriol. 169: 5216.PubMedGoogle Scholar
  39. Peters, J., Peters, M., Lottspeich, F., and Baumeister, W., 1989, S-layer protein gene of Acetogenium kivui: Cloning and expression in Escherichia coli and determination of the nucleotide sequence, J. Bacteriol. 171: 6307.PubMedGoogle Scholar
  40. Peters, J., Rudolf, S., Oschkinat, H., Mengele, R., Sumper, M., Kellermann, J., Lottspeich, F., and Baumeister, W., 1992, Evidence for tyrosine-linked glycosaminoglycan in a bacterial surface protein, Biol. Chem. Hoppe-Seyler 373: 171.PubMedCrossRefGoogle Scholar
  41. Sara, M., Kalsner, I., and Sleytr, U.B., 1988, Surface properties from the S-layer of Clostridium thermosaccharolyticum D120–70 and Clostridium thermohydrosulfuricum L111–69, Arch. Microbiol. 149: 527.PubMedCrossRefGoogle Scholar
  42. Sleytr, U.B., 1978, Regular arrays of macromolecules on bacterial cell walls: Structure, chemistry, assembly, and function, Int. Rev. Cytol. 53: 1.PubMedCrossRefGoogle Scholar
  43. Sleytr, U.B., and Glauert, A.M., 1976, Ultrastructure of the cell walls of two closely related clostridia that possess different regular arrays of surface subunits, J. Bacteriol. 126: 869.PubMedGoogle Scholar
  44. Sleytr, U.B., and Messner, P., 1983, Crystalline surface layers on bacteria, Annu. Rev. Microbiol. 37: 311.PubMedCrossRefGoogle Scholar
  45. Sleytr, U.B., and Thorne, K.J.I., 1976, Chemical characterization of the regularly arrayed surface layers of Clostridium thermosaccharolyticum and Clostridium thermohydrosulfuricum, J. Bacteriol. 126: 377.PubMedGoogle Scholar
  46. Sleytr, U.B., Sara, M., Küpcü, Z., and Messner, P., 1986, Structural and chemical characterization of S-layers of selected strains of Bacillus stearothermophilus and Desulfotomaculum nigrificans, Arch. Microbiol. 146: 19.PubMedCrossRefGoogle Scholar
  47. Sleytr, U.B., Mundt, W., and Messner, P., 1987, Pharmazeutische Struktur, Eur. Patent Application 0 306 473 Al.Google Scholar
  48. Sleytr, U.B., Messner, P., Pum, P., and Sara, M., eds., 1988, “Crystalline Bacterial Cell Surface Layers”, Springer-Verlag, Berlin.Google Scholar
  49. Sleytr, U.B., Messner, P., Pum, D., and Sara, M., 1993, Crystalline bacterial cell surface layers: General principles and application potentials, in:“Symposium Series, Society for Applied Bacteriology”, Blackwell, Oxford, in press.Google Scholar
  50. Smit, J., 1987, Protein surface layers of bacteria, in: “Bacterial Outer Membranes as Model Systems”, M. Inouye, ed., John Wiley and Sons, New York.Google Scholar
  51. Smith, R.H., Messner, P., Lamontagne, LR., Sleytr, U.B., and Unger, F.M., 1993, Induction of T helper cell immunity to oligosaccharide antigens immobilized on crystalline bacterial surface layers (S-layers), Vaccine,in press.Google Scholar
  52. Sumper, M., 1987, Halobacterial glycoprotein biosynthesis, Biochim. Biophys. Acta 906: 69.PubMedCrossRefGoogle Scholar
  53. Wieland, F., Paul, G., and Sumper, M., 1985, Halobacterial flagellins are sulfated glycoproteins, J. Biol. Chem. 260: 15180.PubMedGoogle Scholar
  54. Woese, C.R., Kandler, O., and Wheelis, M.L, 1990, Towards a natural system of organisms: Proposal for the domains archaea, bacteria, and eucarya, Proc. Natl Acad. Sci. USA 87: 4576.PubMedCrossRefGoogle Scholar
  55. Word, N.S., Yousten, A.A., and Howard, L, 1983, Regularly structured and non-regularly structured surface layers of Bacillus sphaericus, FEMS Microbiol. Lett. 17: 277.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Paul Messner
    • 1
  • Judith Schuster - Kolbe
    • 1
  • Christina Schäffer
    • 1
  • Uwe B. Sleytr
    • 1
  • Rudolf Christian
    • 2
  1. 1.Center for Ultrastructure Research and the Ludwig Boltzmann Institute for Molecular NanotechnologyUniversity for AgricultureViennaAustria
  2. 2.Scientific Software CompanyViennaAustria

Personalised recommendations