The structure of secondary cell wall polymers: How Gram-positive bacteria stick their cell walls together

Microbiology

Volumn 151, Issue 3, 2005, Pages 643-651

  Schäffer, Christina ^a   Messner, Paul ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLYCOPROTEIN; PEPTIDOGLYCAN; POLYMER; TEICHOIC ACID;

BACILLACEAE; BACTERIAL CELL WALL; CELL MEMBRANE; CELL SHAPE; CELL SURFACE; CHEMICAL COMPOSITION; GRAM POSITIVE BACTERIUM; MICROBIAL DIVERSITY; NANOTECHNOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOSIS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; SEPARATION TECHNIQUE;

BACILLACEAE; BACTERIAL PROTEINS; CELL WALL; MEMBRANE GLYCOPROTEINS; POLYMERS;

BACTERIA (MICROORGANISMS); POSIBACTERIA;

EID: 15844394070     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.27749-0     Document Type: Review

References (64)

1. Altman, E., Brisson, J.-R., Messner, P. & Sleytr, U. B. (1990). Chemical characterization of the regularly arranged surface layer glycoprotein of Clostridium thermosaccharolyticum D120-70. Eur J Biochem 188, 73-82.
2. Altman, E., Schäffer, C., Brisson, J.-R. & Messner, P. (1996). Isolation and characterization of an amino sugar-rich glycopeptide from the surface layer glycoprotein of Thermoanaerobacterium thermosaccharolyticum E207-71. Carbohydr Res 295, 245-253.
3. Antikainen, J., Anton, L., Sillanpää, J. & Korhonen, T. K. (2002). Domains in the S-layer protein CbsA of Lactobacillus crispatus involved in adherence to collagens, laminin and lipoteichoic acids and in self-assembly. Mol Microbiol 46, 381-394.
4. Araki, Y. & Ito, E. (1989). Linkage units in cell walls of Gram-positive bacteria. CRC Crit Rev Microbiol 17, 121-135.
5. Archibald, A. R., Baddiley, J. & Blumsom, N. L. (1968). The teichoic acids. Adv Enzymol 30, 223-253.
6. Archibald, A. R., Hancock, I. C. & Harwood, C. R. (1993). Cell wall structure, synthesis and turnover. In Bacillus subtilis and Other Gram-Positive Bacteria, pp. 381-410. Edited by A. Sonenshein, J. A. Hoch & R. Losick. Washington, DC: American Society for Microbiology.
7. Baddiley, J. (1972). Teichoic acids in cell walls and membranes of bacteria. Essays Biochem 8, 35-77.
8. Bayer, E. A., Belaich, J.-P., Shoham, Y. & Lamed, R. (2004). The cellulosomes: multienzyme machines for degradation of plant cell wall polysaccharides. Annu Rev Microbiol 58, 521-554.
9. Cava, F., de Pedro, M. A., Schwarz, H., Henne, A. & Berenguer, J. (2004). Binding to pyruvylated compounds as an ancestral mechanism to anchor the outer envelope in primitive bacteria. Mol Microbiol 52, 677-690.
10. Egelseer, E. M., Danhorn, T., Pleschberger, M., Hotzy, C., Sleytr, U. B. & Sára, M. (2001). Characterization of an S-layer glycoprotein produced in the course of S-layer variation of Bacillus stearothermophilus ATCC 12980 and sequencing and cloning of the sbsD gene encoding the protein moiety. Arch Microbiol 177, 70-80.
11. Ellwood, D. C. & Tempest, D. W. (1969). Influence of growth environment on the cell wall anionic polymers in some Gram-positive bacteria. J Gen Microbiol 57, xv.
12. Fischer, W. (1988). Physiology of lipoteichoic acids in bacteria. Adv Microb Physiol 29, 233-302.
13. Fischer, W. (1994). Lipoteichoic acids and lipoglycans. In Bacterial Cell Wall, pp. 199-215. Edited by J.-M. Ghuysen & R. Hakenbeck. Amsterdam: Elsevier.
14. Fujino, T., Béguin, P. & Aubert, J. P. (1993). Organization of a Clostridium thermocellum gene cluster encoding the cellulosomal scaffolding protein CipA and a protein possibly involved in attachment of the cellulosome to the cell surface. J Bacteriol 175, 1891-1899.
15. Hancock, I. C. & Baddiley, J. (1985). Biosynthesis of the bacterial envelope polymers teichoic acid and teichuronic acid. In The Enzymes of Biological Membranes, Vol. 2, 2nd edn, pp. 279-307. Edited by A. N. Martonosi. New York: Plenum.
16. Huber, C., Ilk N., Rünzler, D., Egelseer, E. M., Weigert, S., Sleytr, U. B. & Sára, M. (2005). The three S-layer-like homology motifs of the S-layer protein SbpA of Bacillus sphaericus CCM 2177 are not sufficient for binding to the pyruvylated secondary cell wall polymer. Mol Microbiol 55, 197-205.
17. Ilk, N., Kosma, P., Puchberger, M., Egelseer, E. M., Mayer, H. F., Sleytr, U. B. & Sára, M. (1999). Structural and functional analyses of the secondary cell wall polymer of Bacillus sphaericus CCM 2177 that serves as an S-layer-specific anchor. J Bacteriol 181, 7643-7646.
18. Jarosch, M., Egelseer, E. M., Mattanovich, D., Sleytr, U. B. & Sára, M. (2000). S-layer gene sbsC of Bacillus stearothermophilus ATCC 12980: molecular characterization and heterologous expression in Escherichia coli. Microbiology 146 273-281.
19. Jarosch, M., Egelseer, E. M., Huber, C., Moll, D., Mattanovich, D., Sleytr, U. B. & Sára, M. (2001). Analysis of the structure-function relationship of the S-layer protein SbsC of Bacillus stearothermophilus ATCC 12980 by producing truncated forms. Microbiology 147, 1353-1363.
20. Kuen, B., Sleytr, U. B. & Lubitz, W. (1994). Sequence analysis of the sbsA gene encoding the 130-kDa surface layer protein of Bacillus stearothermophilus strain PV72. Gene 154, 115-120.
21. Kuen, B., Koch, A., Asenbauer, E., Sára, M. & Lubitz, W. (1997). Molecular characterization of the Bacillus stearothermophilus PV72 S-layer gene sbsB induced by oxidative stress. J Bacteriol 179, 1664-1670.
22. Lee, R. T. & Lee, Y. C. (2000). Affinity enhancement by multivalent lectin-carbohydrate interaction. Glycoconjugate J 17 543-551.
23. Liu, S.-Y., Gherardini, F. C., Matuschek, M., Bahl, H. & Wiegel, J. (1996). Cloning, sequencing, and expression of the gene encoding a large S-layer-associated endoxylanase from Thermoanaerobacterium sp. strain JW/SL-YS 485 in Escherichia coli. J Bacteriol 178, 1539-1547.
24. Lupas, A., Engelhardt H., Peters, J., Santarius, U., Volker, S. & Baumeister, W. (1994). Domain structure of the Acetogenium kivui surface layer revealed by electron crystallography and sequence analysis. J Bacteriol 176, 1224-1233.
25. Mader, C., Huber, C., Moll, D., Sleytr, U. B. & Sára, M. (2004). Interaction of the crystalline bacterial cell surface layer protein SbsB and the secondary cell wall polymer of Geobacillus stearothermophilus PV72 assessed by real-time surface plasmon resonance biosensor technology. J Bacteriol 186, 1758-1768.
26. Masuda, K. & Kawata, T. (1985). Reassembly of a regularly arranged protein in the cell wall of Lactobacillus buchneri and its reattachment to cell walls: chemical modification studies. Microbiol Immunol 29, 927-938.
27. Mesnage, S., Tosi-Couture, E., Mock, M. & Fouet, A. (1999). The S-layer homology domain as a means for anchoring heterologous proteins on the cell surface of Bacillus anthracis. J Appl Microbiol 87, 256-260.
28. Mesnage, S., Tosi-Couture, E., Mock M., Gounon, P. & Fouet, A. (1997). Molecular characterization of the Bacillus anthracis S-layer component: evidence that it is the major cell-associated antigen. Mol Microbiol 23, 1147-1155.
29. Mesnage, S., Fontaine, T., Mignot, T., Delepierre, M., Mock, M. & Fouet, A. (2000). Bacterial SLH domain proteins are non-covalently anchored to the cell surface via a conserved mechanism involving wall polysaccharide pyruvylation. EMBO J 19, 4473-4484.
30. Messner, P. & Schäffer, C. (2003). Prokaryotic glycoproteins. In Progress in the Chemistry of Organic Natural Products, vol. 85, pp. 51-124. Edited by W. Herz, H. Falk & G. W. Kirby. Wien: Springer.
31. Messner, P., Sleytr, U. B., Christian, R., Schulz, G. & Unger, F. M. (1987). Isolation and structure determination of a diacetamidodideoxyuronic acid-containing glycan chain from the S-layer glycoprotein of Bacillus stearothermophilus NRS 2004/3a. Carbohydr Res 168, 211-218.
32. Munson, R. S. & Glaser, L. (1981). Teichoic acid and peptidoglycan assembly in Gram-positive organisms. In Biology of Carbohydrates, vol. 1, pp. 91-121. Edited by V. Ginsburg & P. Robbins. New York: Wiley.
33. Naumova, I. B. & Shashkov, A. S. (1997). Anionic polymers in cell walls of Gram-positive bacteria. Biochemistry (English translation of Biokhimya) 62, 809-840.
34. Navarre, W. W. & Schneewind, O. (1999). Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63, 174-229.
35. Novotny, R., Pfoesti, A., Messner, P. & Schäffer, C. (2004). Genetic organization of chromosomal S-layer glycan biosynthesis loci of Bacillaceae. Glycoconjugate J 20, 435-447.
36. Olsthoorn, M. M., Petersen, B. O., Duus, J., Haverkamp, J., Thomas-Oates, J. E., Bock, K. & Holst, O. (2000). The structure of the linkage between the O-specific polysaccharide and the core region of the lipopolysaccharide from Salmonella enterica serovar Typhimurium revisited. Eur J Biochem 267, 2014-2027.
37. Pooley, H. M. & Karamata, D. (1994). Teichoic acid synthesis in Bacillus subtilis: genetic organisation and biological roles. In Bacterial Cell Wall, pp. 187-198. Edited by J.-M. Ghuysen & R. Hakenbeck. Amsterdam: Elsevier.
38. Pum, D., Schuster, B., Sára, M. & Sleytr, U. B. (2004). Functionalisation of surfaces with S-layers. IEE Proc-Nanotechnol 151, 83-86.
39. Raetz, C. R. H. & Whitfield, C. (2002). Lipopolysaccharide endotoxins. Annu Rev Biochem 71, 635-700.
40. Ries, W., Hotzy, C., Schocher, I., Sleytr, U. B. & Sára, M. (1997). Evidence for the N-terminal part of the S-layer protein from Bacillus stearothermophilus PV72/p2 recognizes a secondary cell wall polymer. J Bacteriol 179, 3892-3898.
41. Rogers, H. J., Perkins, H. R. & Ward, J. B. (1980). Microbial Cell Walls and Membranes. London: Chapman & Hall.
42. Sampathkumar, P. & Gilchrist, M. L. (2004). Synthesis and characterization of bioconjugates of S-layer proteins. Bioconjugate Chem 15, 685-693.
43. Sára, M. (2001). Conserved anchoring mechanisms between crystalline cell surface S-layer proteins and secondary cell wall polymers in Gram-positive bacteria. Trends Microbiol 9, 47-49.
44. Sára, M., Egelseer, E. M., Dekitsch, C. & Sleytr, U. B. (1998b). Identification of two binding domains, one for peptidoglycan and another for a secondary cell wall polymer on the N-terminal part of the S-layer protein SbsB from Bacillus stearothermophilus PV72/p2. J Bacteriol 180, 6780-6783.
45. Sára, M., Dekitsch, C., Mayer, H. F., Egelseer, E. M. & Sleytr, U. B. (1998a). Influence of the secondary cell wall polymer on the reassembly, recrystallization, and stability properties of the S-layer protein from Bacillus stearothermophilus PV72/p2. J Bacteriol 180, 4146-4153.
46. Schäffer, C. & Messner, P. (2004). Surface-layer glycoproteins: an example for the diversity of bacterial glycosylation with promising impacts on nanobiotechnology. Glycobiology 14, 31R-42R.
47. Schäffer, C., Kählig, H., Christian, R., Schulz, G., Zayni, S. & Messner, P. (1999). The diacetamidodideoxyuronic-acid-containing glycan chain of Bacillus stearothermophilus NRS 2004/3a represents the secondary cell wall polymer of wild-type B. stearothermophilus strains. Microbiology 145, 1575-1583.
48. Schäffer, C., Müller, N., Mandal, P. K., Christian, R., Zayni, S. & Messner, P. (2000). A pyrophosphate bridge links the pyruvate-containing secondary cell wall polymer of Paenibacillus alvei CCM 2051 to muramic acid. Glycoconjugate J 17, 681-690.
49. Schäffer, C., Graninger, M. & Messner, P. (2001). Prokaryotic glycosylation. Proteomics 1, 248-261.
50. Schäffer, C., Wugeditsch, T., kählig, H., Scheberl, A., Zayni, S. & Messner, P. (2002). The surface layer (S-layer) glycoprotein of Geobacillus stearothermophilus NRS 2004/3a. Analysis of its glycosylation. J Biol Chem 277, 6230-6239.
51. Schäffer, C., Steindl, C., Müller, N. & Messner, P. (2004). Structural biology of secondary cell wall polymers of S-layer glycoprotein-carrying bacteria. In Proceedings of the 22nd International Carbohydrate Symposium, Glasgow, abstract C33.
52. Sleytr, U. B. (1976). Self-assembly of the hexagonally and tetragonally arranged subunits of bacterial surface layers and their reattachment to cell walls. J Ultrastruct Res 55, 360-377.
53. Sleytr, U. B. (1978). Regular arrays of macromolecules on bacterial cell walls: structure, chemistry, assembly, and function. Int Rev Cytol 53, 1-64.
54. Sleytr, U. B., Messner, P., Pum, D. & Sára, M. (editors) (1996). Crystalline Bacterial Cell Surface Proteins. Austin, TX: R. G. Landes/Academic Press.
55. Sleytr, U. B., Sára, M., Pum, D., Schuster, B., Messner, P. & Schäffer, C. (2002). Self-assembly protein systems: microbial S-layers. In Biopolymers, vol. 7, Polyamides and Complex Proteinaceous Matrices I, pp. 285-338. Edited by A. Steinbüchel & S. R. Fahnestock. Weinheim: Wiley-VCH.
56. Smit, E., Oling, F., Demel, R., Martinez, B. & Pouwels, P. H. (2001). The S-layer protein of Lactobacillus acidophilus ATCC 4356: identification and characterisation of domains responsible for S-protein assembly and cell wall binding. J Mol Biol 305, 245-257.
57. Steindl, C., Schäffer, C., Wugeditsch, T., Graninger, M., Matecko, I., Müller, N. & Messner, P. (2002). The first biantennary bacterial secondary cell wall polymer from bacteria and its influence on S-layer glycoprotein assembly. Biochem J 368, 483-494.
58. Sumper, M. & Wieland, F. T. (1995). Bacterial glycoproteins. In Glycoproteins, pp. 455-473. Edited by J. Montreuil, J. F. G. Vliegenthart & H. Schachter. Amsterdam: Elsevier.
59. Sutherland, I. W. (1999). Microbial polysaccharide products. Biotechnol Genet Eng Rev 16, 217-229.
60. Varki, A., Cummings, R., Esko, J., Freeze, H., Hart, G. & Marth, J. (editors) (1999). Essentials of Glycobiology. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
61. Ward, J. B. (1981). Teichoic and teichuronic acids: biosynthesis, assembly and location. Microbiol Rev 45, 211-243.
62. Wing, C., Kannathasan, V. S., Preston, A., Maskell, D., Wenzel, C. Q., Lam, J. S., Naismith, J. H. & Field, R. A. (2004). Characterization of WlbA (a putative 3-dehydrogenase) and WlbC (a putative 3-transaminase): two key enzymes involved in Bordetella pertussis UDP D-Man-diNAcA biosynthesis. Proceeding of the 22nd International Carbohydrate Symposium, Glasgow, abstract P431.
63. Wugeditsch, T. (1998). Strukturanalyse des S-Schichtglykoproteinglykans und Zellwand-Aminozuckerpolymers von Aneurinibacillus thermoaerophilus DSM 10155. Doctoral thesis, Universität für Bodenkultur Wien.
64. Yamamori, S., Murazumi, N., Araki, Y. & Ito, E. (1978). Formation and function of N-acetylglucosamine-linked phosphoryl- and pyrophosphorylundecaprenols in membranes from Bacillus cereus. J Biol Chem 253, 6516-6522.