Abstract
Bacillus anthracis is a Gram-positive bacterium harboring a complex parietal architecture. The cytoplasmic membrane is surrounded by a thick peptidoglycan of the A1γ type. Only one associated polymer, a polysaccharide composed of galactose, N-acetylglucosamine, and N-acetylmannosamine, is covalently linked to the peptidoglycan. Outside the cell wall is an S-layer. Two proteins can each compose the S-layer. They are noncovalently anchored to the cell wall polysaccharide by their SLH N-terminal domain. The poly-γ-d-glutamate capsule, which covers the S-layer, has an antiphagocytic role and its synthesis is dependent on environmental factors mimicking the mammalian host, such as bicarbonate and a temperature of 37°C.
Keywords
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.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
Ascoli A (1911) Die Präzipitindiagnose bei Milzbrand. Zentralbl Bakt Paras Infekt Krank I orig 58: 63–69
Ashiuchi M, Soda K, Misono H (1999) A poly-y-glutamate synthetic system of Bacillus subtilis IFO 3336: gene cloning and biochemical analysis of poly-y-glutamate produced by Escherichia coli clone cells. Biochem Biophys Res Commun 263: 6–12
Atrih A, Zollner P,Allmaier G, Williamson MP, Foster SJ (1998) Peptidoglycan structural dynamics during germination of Bacillus subtilis 168 endospores. J Bacteriol 180: 4603–4612
Avakyan AA, Katz LN, Levina KN, Pavlova IB (1965) Structure and composition of the Bacillus anthracis capsule. J Bacteriol 90: 1082–1095
Bail O (1915) Veränderung der Bakterien in Tierkörper. Ueber die Korrelation zwischen Kapselbildung Sporenbildung und Infektiosität des Milzbrandbazillus. Zentralbl Bakt Paras Infekt Krank I orig 75: 159–173
Beveridge TJ, Graham LL (1991) Surface layers of bacteria. Microbiol Rev 55: 684–705
Bishop DG, Rutberg L, Samuelson B (1967) The chemical composition of the cytoplasmic membrane of Bacillus subtilis. Eur J Biochem 2: 448–453
Brückner V, Kovacs J (1953) Structure of poly-d-glutamic acid isolated from capsulated strains of Bacillus anthracis. Nature 172: 508
Burger M (1950) Anthrax polysaccharides. In: Thomas CC (ed) Bacterial Polysaccharides Springfield, USA, pp 121–134
Chauvaux S, Matuschek M, Beguin P (1999) Distinct affinity of binding sites for S-layer homologous domains in Clostridium thermocellum and Bacillus anthracis cell envelopes. J Bacteriol 181: 2455–2458
Cromartie WJ, Bloom WL, Watson DW (1946a) Studies on infection with Bacillus anthracis. I. A histopathological study of skin lesions produced by Bacillus anthracis in susceptible and resistant animal species. J Infect Dis 80: 1–13
Cromartie WJ, Watson DW, Bloom WL, Heckly RJ (1946b) Studies on infection with Bacillus anthracis. II. The immunological and tissue damaging properties of extracts prepared from lesions of Bacillus anthracis infection. J Infect Dis 80: 14–27
De Mendoza D, Farias R (1988) Effects of fatty acid supplementation on membrane fluidity in microorganisms. In: Aloia RC, Curtain CC, Gordon LM (eds) Physiological Regulation of Membrane Fluidity. Alan R. Liss, Inc. New York, Vol 3, pp 119–149
De Mendoza D, Grau R, Cronan Jr. JE (1993) Biosynthesis and function of membrane lipids. In: Sonenshein AL, Hoch JA, Losick R (eds) Bacillus subtilis and other gram-positive bacteria. American Society for Microbiology Washington, DC, pp 411–421
Doyle RJ, Koch AL (1987) The functions of autolysins in the growth and division of Bacillus subtilis. Crit Rev Microbiol 15: 169–222
Eastin JD, Thorne CB (1963) Carbon dioxide fixation in Bacillus anthracis. J Bacteriol 85: 410–417
Ekwunife FS, Singh J, Taylor KG, Doyle RJ (1991) Isolation and purification of cell wall polysaccharide of Bacillus anthracis (A Sterne). FEMS Microbiol Lett 82:257– 262
Ellwood DC, Tempest DW (1972) Effects of environment on bacterial wall content and composition. Adv Microbiol Physiol 7: 83–117
Etienne-Toumelin I, Sirard J-C, Duflot E, Mock M, Fouet A (1995) Characterization of the Bacillus anthracis S-layer: cloning and sequencing of the structural gene. J Bacteriol 177: 614–620
Ezzell Jr. JW, Abshire TG (1988) Immunological analysis of cell-associated antigens of Bacillus anthracis. Infect Immun 56: 349–356
Ezzell Jr. JW, Abshire TG, Little SF, Lidgarding BC, Brown C (1990) Identification of Bacillus anthracis by using monoclonal antibody to cell wall galactoseN-acetylglucosamine polysaccharide. J Clin Microbiol 28: 223–231
Ezzell JW, Abshire TG (1996) Encapsulation of Bacillus anthracis spores and spore identification. In: Turnbull, PCB (ed), Proceedings of the International Workshop on Anthrax. Salisbury Medical Bulletin, Special Supplement n° 87, p. 42
Fox A, Black GE, Fox K, Rostovtseva S (1993) Determination of carbohydrate profiles of Bacillus anthracis and Bacillus cereus including identification of O-methyl methylpentoses by using gas chromatography-mass spectrometry. J Clin Microbiol 31: 887–894
Gardner JM, Troy FA (1979) Chemistry and biosynthesis of the poly (g-d-glutamyl) capsule in Bacillus licheniformis. Activation, racemization, and polymerization of glutamic acid by a membranous polyglutamyl synthetase complex. J Biol Chem 254: 6262–6269
Gerhardt P (1967) Cytology of Bacillus anthracis. Fed Proc 26: 1504–1517
Ghuysen J-M (1968) Use of bacteriolytic enzymes in determination of wall structure and their role in cell metabolism. Bacteriol Rev 32: 425–464
Goodman JW, Nitecki DE (1967) Studies on the relation of a prior immune response to immunogenicity. Immunology 13: 577–583
Graham LL, Beveridge TJ (1994) Structural differentiation of the Bacillus subtilis 168 cell wall. J Bacteriol 176: 1413–1421
Green BD, Battisti L, Koehler TM, Thorne CB, Iv ins BE (1985) Demonstration of a capsule plasmid in Bacillus anthracis. Infect Immun 49: 291–297
Guffanti AA, Clejan S, Falk LH, Hicks DB, Krulwich TA (1987) Isolation and characterization of uncoupler resistant mutants of Bacillus subtilis. J Bacteriol 169: 4479–4485
Haldenwang WG (1995) The sigma factors of Bacillus subtilis. Microbiol Rev 59: 1–30
Hanby WE, Rydon HN (1946) The capsular susbtance of Bacillus anthracis. Biochem J 40: 297–309
Hancock IC (1983) Activation and inactivation of secondary wall polymers in Bacillus subtilis W23. Arch Microbiol 134: 222–226
Hancock IC (1997) Bacterial cell surface carbohydrates: structure and assembly. Biochem Soc Trans 25: 183–187
Holt SC, Leadbetter ER (1969) Comparative ultrastructure of selected aerobic spore-forming bacteria: a freeze-etching study. Bacteriol Rev 33: 346–378
Huang X, Helmann JD (1998) Identification of target promoters for the Bacillus subtilis sX factor using a consensus-directed search. J Mol Biol 279: 165–173
Ivánovics G, Brückner V (1937a) Notiz zu unserer Mitteilung: chemische und immunologische Studien über den Mechanismus der Milzbrandinfektion und Immunität. Zeitschr Immunitätsf 91: 175–176
Ivánovics G, Brückner V (1937b) Chemische und immunologische Studien über den Mechanismus der Milzbrandinfektion und Immunität. Zeitschr Immunitätsf 90: 304–318
Iwasaki H, Shimada A, Yokoyama K, Ito E (1989) Structure and glycosylation of lipoteichoic acids in Bacillus strains. J Bacteriol 171: 424–429
Jolliffe LK, Doyle RJ, Streips UN (1981) The energized membrane and cellular autolysis in Bacillus subtilis. Cell 25: 753–763
Kaneda T (1991) Iso-and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol Rev 55: 288–302
Kawata T, Takeoka A, Takumi K, Masuda K (1984) Demonstration and preliminary characterization of a regular array in the cell wall of Clostridium difficile. FEMS Microbiol Lett 24: 323–328
Koch AL, Doyle RJ (1985) Inside-to-outside growth and turnover of the wall of gram-positive rods. J Theor Biol 117: 137–157
König H, Niemetz R (1997) Polyglutamate surface polypeptides in Bacteria and Archae. FEMS Microbiol Rev 20: 36–39
Kotiranta A, Haapasalo M, Kari K, Kerosuo E, Olsen I, Sorsa T, Meurman JH, Lounatmaa K (1998) Surface structure, hydrophobicity, phagocytosis, and adherence to matrix proteins of Bacillus cereus cells with and without the crystalline surface protein layer. Infect Immun 66: 4895–4902
Kramar E (1922) Untersuchungen über die chemische Beschaffenheit der Kapsel- substanz einiger Kapselbakterien. Centralbl f Bakt I Abt Originale 87: 401–406
Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, Bertero MG, Bessieres P, Bolotin A, Borchert S, Borris R, Boursier L, Brans A, Braun M, Brignell SC, Bron S, Brouillet S, Bruschi CV, Caldwell B, Capuano V, Carter NM, Choi SK, Codani JJ, Connerton IF, Danchin A (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390: 237–238
Kuroda A, Asami Y, Sekiguchi J (1993) Molecular cloning of a sporulation-specific cell wall hydrolase gene of Bacillus subtilis. J Bacteriol 175: 6260–6268
Lawrence D, Heitefuss S, Seifert HS (1991) Differentiation of Bacillus anthracis from Bacillus cereus by gas chromatographic whole-cell fatty acid analysis. J Clin Microbiol 29: 1508–1512
Lemaire M, Ohayon H, Gounon P, Fujino T, Béguin P (1995) OlpB, a new outer layer protein of Clostridium thermocellum, and binding of its S-layer-like domains to components of the cell envelope. J Bacteriol 177: 2451–2459
Lennarz WJ (1970) Bacterial lipids. In: Wakil JJ (ed) Lipid Metabolism. Academic Press, Inc. New York
Leonard CG, Housewright RD (1963) Polyglutamic acid synthesis by cell-free extracts of Bacillus licheniformis. Biochim Biophys Acta 73: 530–532
Lindeque PM, Turnbull PC (1994) Ecology and epidemiology of anthrax in the Etosha National Park, Namibia. Onderstepoort J Vet Res 61: 71–83
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
Makino SI, Uchida I, Terakado N, Sasakawa C, Yoshikawa M (1989) Molecular characterization and protein analysis of the cap region, which is essential for encapsulation in Bacillus anthracis. J Bacteriol 171: 722–730
Maurer PH (1965) Antigenicity of polypeptides (poly alpha amino acids). XIII. Immunological studies with synthetic polymers containing only d-or d-and l-aamino acids. J Exp Med 121: 339–349
Merad T, Archibald AR, Hancock IC, Harwood CR, Hobot JA (1989) Cell wall assembly in Bacillus subtilis: visualization of old and new wall material by electron microscopic examination of samples stained selectively for teichoic acid and teichuronic acid. J Gen Microbiol 135: 645–655
Mesnage S, Fontaine T, Mignot T, Delepierre M, Mock M, and 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
Mesnage S, Tosi Couture E, Mock M, Fouet A (1999a) 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
Mesnage S, Tosi-Couture E, Gounon P, Mock M, Fouet A (1998) The capsule and S-layer: two independent and yet compatible macromolecular structures in Bacillus anthracis. J Bacteriol 180: 52–58
Mesnage S, Tosi-Couture E, Mock M, Gounon P, Fouet A (1997) Molecular characterization of the Bacillus anthracis main S-layer component: evidence that it is the major cell-associated antigen. Mol Microbiol 23: 1147–1155
Mesnage S, Weber-Levy M, Haustant M, Mock M, Fouet A (1999b) Cell surface-exposed tetanus toxin fragment C produced by recombinant Bacillus anthracis protects against tetanus toxin. Infect Immun 67: 4847–4850
Messner P, Sleytr UB (1992) Crystalline bacterial cell-surface layers. Adv Microb Physiol 33: 212–275
Meynell E, Meynell GG (1964) The roles of serum and carbon dioxide in capsule formation by Bacillus anthracis. J Gen Microbiol 34: 153–164
Meynell GG, Meynell E (1966) The biosynthesis of poly D-glutamic acid, the capsular material of Bacillus anthracis. J Gen Microbiol 43: 119–138
Mignot T, Mesnage S, Couture-Tosi E, Mock M, Fouet A (2002) Developmental switch of S-layer protein synthesis in Bacillus anthracis. Mol Microbiol 43: 1615–1627
Molnár J, Prágai B (1971) Attempts to detect the presence of teichoic acid in Bacillus anthracis. Acta Microbiol Acad Sci Hung 18: 105–108
Okinaka RT, Cloud K, Hampton O, Hoffmaster AR, Hill KK, Keim P, Koehler TM, Lamke G, Kumano S, Mahillon J, Manter D, Martinez Y, Ricke D, Svensson R, Jackson PJ (1999) Sequence and organization of pXO1, the large Bacillus anthracis plasmid harboring the anthrax toxin genes. J Bacteriol 181: 6509–6515
Olabarría G, Carrascosa JL, de Pedro MA, Berenguer J (1996) A conserved motif in S-layer proteins is involved in peptidoglycan binding in Thermus thermophilus. J Bacteriol 178: 4765–4772
Parker CW, Thiel JA, Mitchell S (1965) The immunogenicity of hapten-polylysine conjugates. J Immunol 94: 289–294
Pooley HM (1976) Layered distribution, according to age, within the cell wall of Bacillus subtilis. J Bacteriol 125: 1139–1147
Preisz H (1909) Experimentelle Studien über Virulenz, Empfänglichkeit und Immunität beim Milzbrand. Zeitschr Immunitätsf 5: 341–452
Quinn CP, Turnbull PCB (1998) Anthrax. In: Hausler Jr WJ, Sussman M (eds) Microbiology and Microbial Infections: Bacterial Infections. Topley and Wilson’s, Ninth edition London, Sydney, Auckland, Vol 3, pp 799–818
Ray KC, Mesnage S, Washburn R, Mock M, Fouet A, Blaser M (1998) Complement binding to Bacillus anthracis mutants lacking surface structures. Abstracts Book Poster 98th General Meeting. American Society for Microbiology Atlanta, Georgia, USA, pp B-418
Record BR, Wallis RG (1956) Physicochemical examination of polyglutamic acid from Bacillus anthracis grown in vivo. Biochem J 63: 443–447
Ries W, Hotzy C, Schocher I, Sleytr UB, Sára M (1997) Evidence that 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
Roelants GE, Senyk G, Goodman JW (1969) Immunochemical studies on the polyg-d-glutamyl capsule of Bacillus anthracis. V. The in vivo fate and distribution in rabbits of the polypeptide in immunogenic and nonimmunogenic forms. Israel J Med Sci 5: 196–208
Roth IL, Lewis J, CWL, Williams RP (1960) Electron microscope study of Bacillus anthracis in mouse spleen. J Bacteriol 80: 772–782
Roth IL, Williams RP (1964) Nature of the cytopathic area surrounding virulent cells of Bacillus anthracis in mouse spleen. J Bacteriol 88: 523–530
Salton MRJ (1994) The bacterial cell envelope–a historical perspective. In: Ghuysen J-M, Hakenbeck R (eds.) The Bacterial Cell Wall. Elsevier Science B.V. Amsterdam, The Netherlands, Vol 27, pp 1–22
Sára M, Kuen B, Mayer HF, Mandl F, Schuster KC, Sleytr UB (1996) Dynamics in oxygen-induced changes in S-layer protein synthesis from Bacillus stearothermophilus PV72 and the S-layer-deficient variant T5 in continuous culture and studies of the cell wall composition. J Bacteriol 178: 2108–2117
Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36: 407–477
Sekiguchi J, Akeo K, Yamamoto H, Khasanov FK, Alonso JC, Kuroda A (1995) Nucleotide sequence and regulation of a new putative cell wall hydrolase gene, cwlD, which affects germination in Bacillus subtilis. J Bacteriol 177:5582– 5589
Shockman GD, Barrett JF (1983) Structure, function and assembly of cell walls of gram-positive bacteria. Ann Rev Microbiol 37: 501–527
Shockman GD, Höltje J-V (1994) Microbial peptidoglycan (murein) hydrolases. In: Ghuysen J-M, Hakenbeck R (eds) Bacterial Cell Wall. Elsevier Science B.V. Amsterdam, The Netherlands, Vol 27, pp 131–166
Simonen M, Palva I (1993) Protein secretion in Bacillus species. Microbiol Rev 57: 109–137
Sleytr UB, Messner P (1983) Crystalline surface layers on bacteria. Ann Rev Microbiol 37: 311–339
Sleytr UB, Messner P, Pum D, Sara M (1993) Crystalline bacterial cell surface layers. Mol Microbiol 10: 911–916
Sleytr UB, Messner P, Pum D, Sara M (1996) Occurrence, location, ultrastructure and morphogenesis of S-Layers. In: Sleytr UW, Messner P, Pum D, Sara M (eds) Crystalline Bacterial Cell Surface Proteins. Academic Press New York, pp 5–33
Smith TJ, Blackman SA, Foster SJ (1996) Peptidoglycan hydrolases of Bacillus subtilis 168. Microb Drug Resist 2: 113–118
Soldo B, Lazarevic V, Pagni M, Karamata D (1999) Teichuronic acid operon of Bacillus subtilis 168. Mol Microbiol 31: 795–805
Takumi K, Koga T, Oka T, Endo Y (1991) Self-assembly, adhesion, and chemical properties of tetragonarly arrayed S-layer proteins of Clostridium. J Gen Appl Microbiol 37: 455–465
Thorne CB (1956) Capsule formation and glutamyl polypeptide synthesis by Bacillus anthracis and Bacillus subtilis. In: Spooner ETC, Stocker BAD (eds) Bacterial Anatomy. Cambridge University Press Cambridge, pp 68–80
Thorne CB (1993) Bacillus anthracis. In: Sonenshein AL, Hoch JA, Losick R (eds) Bacillus subtilis and other Gram-positive Bacteria. American Society for Microbiology Washington, DC, pp 113–124
Thorne CB, Leonard CG (1958) Isolation of d-and l-glutamyl polypeptides from culture filtrates of Bacillus subtilis. J Biol Chem 233: 1109–1112
Tomcsik J (1956) Bacterial capsules and their relation to the cell wall. In: Spooner ETC, Stocker BAD (eds.) Bacterial Anatomy. Cambridge University Press Cambridge, pp 41–67
Tomcsik J, Szongott H (1933) Ueber ein spezifisches Protein der Kapsel des Milzbrandbazillus. Zeitschr Immunitätsf 78: 86–99
Troy FA (1973a) Chemistry and biosynthesis of the poly (y-D-glutamyl) capsule in Bacillus licheniformis. I. Properties of the membrane mediated biosynthetic reaction. J Biol Chem 248:305–315
Troy FA (1973b) Chemistry and biosynthesis of the poly (y-D-glutamyl) capsule in Bacillus licheniformis. II. Characterization and structural properties of the enzymatically synthesis polymer. J Biol Chem 248: 316–324
Tsuboi A, Tsukagoshi N, Udaka S (1982) Reassembly in vitro of hexagonal surface arrays in a protein-producing bacterium, Bacillus brevis 47. J Bacteriol 151:1485– 1497
Uchida I, Makino S, Sasakawa C,Yoshikawa M, Sugimoto C, Terakado N (1993) Identification of a novel gene, dep, associated with depolymerization of the capsular polymer in Bacillus anthracis. Mol Microbiol 9: 487–496
Uchida I, Sekizaki T, Hashimoto K, Terakado N (1985) Association of the encapsulation of Bacillus anthracis with a 60-megadalton plasmid. J Gen Microbiol 131: 363–367
Vanden Boom T, Cronan Jr. JE (1989) Genetics and regulation of bacterial lipid metabolism. Annu Rev Microbiol 43: 317–343
Welkos SL (1991) Plasmid-associated virulence factors of non-toxigenic (pXO1–) Bacillus anthracis. Microb Pathog 10: 183–198
Zipperle Jr. GF, Ezzell Jr. J, Doyle RJ (1984) Glucosamine substitution and muramidase susceptibility in Bacillus anthracis. Can J Microbiol 30: 553–559
Zwartouw HT, Smith H (1956) Polyglutamic acid from Bacillus anthracis grown in vivo: structure and aggressin activity. Biochem J 63: 437–454
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2002 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Fouet, A., Mesnage, S. (2002). Bacillus anthracis Cell Envelope Components. In: Koehler, T.M. (eds) Anthrax. Current Topics in Microbiology and Immunology, vol 271. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-05767-4_5
Download citation
DOI: https://doi.org/10.1007/978-3-662-05767-4_5
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-07799-9
Online ISBN: 978-3-662-05767-4
eBook Packages: Springer Book Archive