1932

Abstract

, the anthrax agent, is a member of the sensu lato group, which includes invasive pathogens of mammals or insects as well as nonpathogenic environmental strains. The genes for anthrax pathogenesis are located on two large virulence plasmids. Similar virulence plasmids have been acquired by other strains and enable the pathogenesis of anthrax-like diseases. Among the virulence factors of is the S-layer-associated protein BslA, which endows bacilli with invasive attributes for mammalian hosts. BslA surface display and function are dependent on the bacterial S-layer, whose constituents assemble by binding to the secondary cell wall polysaccharide (SCWP) via S-layer homology (SLH) domains. and other pathogenic isolates harbor genes for the secretion of S-layer proteins, for S-layer assembly, and for synthesis of the SCWP. We review here recent insights into the assembly and function of the S-layer and the SCWP.

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2017-09-08
2024-06-18
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Literature Cited

  1. Aanensen DM, Mavroidi A, Bentley SD, Reeves PR, Spratt BG. 1.  2007. Predicted functions and linkage specificities of the products of the Streptococcus pneumoniae capsular biosynthetic loci. J. Bacteriol. 189:7856–76 [Google Scholar]
  2. Agaisse H, Gominet M, Økstad OA, Kolstø AB, Lereclus D. 2.  1999. PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis. Mol. Microbiol. 32:1043–53 [Google Scholar]
  3. Agrawal A, Lingappa J, Leppla SH, Agrawal S, Jabbar A. 3.  et al. 2003. Impairment of dendritic cells and adaptive immunity by anthrax lethal toxin. Nature 424:329–34 [Google Scholar]
  4. Albers SV, Meyer BH. 4.  2011. The archaeal cell envelope. Nat. Rev. Microbiol. 9:414–26 [Google Scholar]
  5. Anderson VJ, Kern JW, McCool JW, Schneewind O, Missiakas DM. 5.  2011. The SLH domain protein BslO is a determinant of Bacillus anthracis chain length. Mol. Microbiol. 81:192–205 [Google Scholar]
  6. Antonation KS, Grützmacher K, Dupke S, Mabon P, Zimmermann F. 6.  et al. 2016. Bacillus cereus biovar anthracis causing anthrax in sub-Saharan Africa—chromosomal monophyly and broad geographic distribution. PLOS Negl. Trop. Dis. 10:e0004923 [Google Scholar]
  7. Balderas MA, Nobles CL, Honsa ES, Alicki ER, Maresso AW. 7.  2012. Hal is a Bacillus anthracis heme acquisition protein. J. Bacteriol. 194:5513–21 [Google Scholar]
  8. Baranova E, Fronzes R, Garcia-Pino A, Van Gerven N, Papapostolou D. 8.  et al. 2012. SbsB structure and lattice reconstruction unveil Ca2+ triggered S-layer assembly. Nature 487:119–22 [Google Scholar]
  9. Bartkus JM, Leppla SH. 9.  1989. Transcriptional regulation of the protective antigen gene of Bacillus anthracis. Infect. Immun. 57:2295–300 [Google Scholar]
  10. Bentley SD, Aanensen DM, Mavroidi A, Saunders D, Rabbinowitsch E. 10.  et al. 2006. Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLOS Genet 2:e31 [Google Scholar]
  11. Bouillaut L, Perchat S, Arold S, Zorrilla S, Slamti L. 11.  et al. 2008. Molecular basis for group-specific activation of the virulence regulator PlcR by PapR heptapeptides. Nucleic Acids Res 36:3791–801 [Google Scholar]
  12. Bourgogne A, Drysdale M, Hilsenbeck SG, Peterson SN, Koehler TM. 12.  2003. Global effects of virulence gene regulators in a Bacillus anthracis strain with both virulence plasmids. Infect. Immun. 71:2736–43 [Google Scholar]
  13. Boydston JA, Chen P, Steichen CT, Turnbough CLJ. 13.  2005. Orientation within the exosporium and structural stability of the collagen-like glycoprotein BclA of Bacillus anthracis. J. Bacteriol. 187:5310–17 [Google Scholar]
  14. Bradley KA, Mogridge J, Mourez M, Collier RJ, Young JA. 14.  2001. Identification of the cellular receptor for anthrax toxin. Nature 414:225–29 [Google Scholar]
  15. Braunstein M, Brown AM, Kurtz S, Jacobs WRJ. 15.  2001. Two nonredundant SecA homologues function in mycobacteria. J. Bacteriol. 183:6979–90 [Google Scholar]
  16. Brézillon C, Haustant M, Dupke S, Corre JP, Lander A. 16.  et al. 2015. Capsules, toxins and AtxA as virulence factors of emerging Bacillus cereus biovar anthracis. PLOS Negl. Trop. Dis. 9:e0003455 [Google Scholar]
  17. Bruckner V, Kovacs J, Denes G. 17.  1953. Structure of poly-d-glutamic acid isolated from capsulated strains of B. anthracis. Nature 172:508 [Google Scholar]
  18. Candela T, Fouet A. 18.  2005. Bacillus anthracis CapD, belonging to the γ-glutamyltranspeptidase family, is required for the covalent anchoring of capsule to peptidoglycan. Mol. Microbiol. 57:717–26 [Google Scholar]
  19. Candela T, Maes E, Garenaux E, Rombouts Y, Krzewinski F. 19.  et al. 2011. Environmental and biofilm-dependent changes in a Bacillus cereus secondary cell wall polysaccharide. J. Biol. Chem. 286:31250–62 [Google Scholar]
  20. Candela T, Mock M, Fouet A. 20.  2005. CapE, a 47-amino-acid peptide, is necessary for Bacillus anthracis polyglutamate capsule synthesis. J. Bacteriol. 187:7765–72 [Google Scholar]
  21. Chan YGY, Frankel MB, Dengler V, Schneewind O, Missiakas DM. 21.  2013. Staphylococcus aureus mutants lacking the LytR-CpsA-Psr (LCP) family of enzymes release wall teichoic acids into the extracellular medium. J. Bacteriol. 195:4650–59 [Google Scholar]
  22. Choudhury B, Leoff C, Saile E, Wilkins P, Quinn CP. 22.  et al. 2006. The structure of the major cell wall polysaccharide of Bacillus anthracis is species specific. J. Biol. Chem. 281:27932–41 [Google Scholar]
  23. Couture-Tosi E, Delacroix H, Mignot T, Mesnage S, Chami M. 23.  et al. 2002. Structural analysis and evidence for dynamic emergence of Bacillus anthracis S-layer networks. J. Bacteriol. 184:6448–56 [Google Scholar]
  24. Daffonchio D, Cherif A, Brusetti L, Rizzi A, Mora D. 24.  et al. 2003. Nature of polymorphisms in 16S-23S rRNA gene intergenic transcribed spacer fingerprinting of Bacillus and related genera. Appl. Environ. Microbiol. 69:5128–37 [Google Scholar]
  25. Dalbey RE, Wickner W. 25.  1985. Leader peptidase catalyzes the release of exported proteins from the outer surface of the Escherichia coli plasma membrane. J. Biol. Chem. 260:15925–31 [Google Scholar]
  26. D'Elia MA, Henderson JA, Beveridge TJ, Heinrichs DE, Brown ED. 26.  2009. The N-acetylmannosamine transferase catalyzes the first committed step of teichoic acid assembly in Bacillus subtilis and Staphylococcus aureus. J. Bacteriol 191:4030–34 [Google Scholar]
  27. Dong S, Chesnokova ON, Turnbough CLJ, Pritchard DG. 27.  2009. Identification of the UDP-N-acetylglucosamine 4-epimerase involved in exosporium protein glycosylation in Bacillus anthracis. J. Bacteriol. 191:7094–101 [Google Scholar]
  28. Drysdale M, Bourgogne A, Hilsenbeck SG, Koehler TM. 28.  2004. atxA controls Bacillus anthracis capsule synthesis via acpA and a newly discovered regulator, acpB. J. Bacteriol 186:307–15 [Google Scholar]
  29. Drysdale M, Bourgogne A, Koehler TM. 29.  2005. Transcriptional analysis of the Bacillus anthracis capsule regulators. J. Bacteriol. 187:5108–14 [Google Scholar]
  30. Drysdale M, Heninger S, Hutt J, Chen Y, Lyons CR, Koehler TM. 30.  2005. Capsule synthesis by Bacillus anthracis is required for dissemination in murine inhalation anthrax. EMBO J 24:221–27 [Google Scholar]
  31. Duesbery NS, Webb CP, Leppla SH, Gordon VM, Klimpel KR. 31.  et al. 1998. Proteolytic inactivation of Map-kinase-kinase by anthrax lethal factor. Science 280:734–37 [Google Scholar]
  32. Duong F, Wickner W. 32.  1997. The SecDFyajC domain of preprotein translocase controls preprotein movement by regulating SecA membrane cycling. EMBO J 16:4871–79 [Google Scholar]
  33. Ebrahimi CM, Kern JW, Sheen TR, Ebrahimi-Fardooee MA, van Sorge NM. 33.  et al. 2009. Penetration of the blood-brain barrier by Bacillus anthracis requires the pXO1-encoded BslA protein. J. Bacteriol. 191:7165–73 [Google Scholar]
  34. Economou A, Pogliano JA, Beckwith J, Oliver DB, Wickner W. 34.  1995. SecA membrane cycling at SecYEG is driven by distinct ATP binding and hydrolysis events and is regulated by SecD and SecF. Cell 83:1171–81 [Google Scholar]
  35. Economou A, Wickner W. 35.  1994. SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78:835–43 [Google Scholar]
  36. Endo A, Rothfield L. 36.  1969. Studies of a phospholipid-requiring bacterial enzyme: I. Purification and properties of uridine diphosphate galactose; lipopolysaccharide alpha-3-galactosyl transferase. Biochemistry 8:3500–7 [Google Scholar]
  37. Etienne-Toumelin I, Sirard JC, Duflot E, Mock M, Fouet A. 37.  1995. Characterization of the Bacillus anthracis S-layer: cloning and sequencing of the structural gene. J. Bacteriol. 177:614–20 [Google Scholar]
  38. Ezzell JWJ, Abshire TG, Little SF, Lidgerding BC, Brown C. 38.  1990. Identification of Bacillus anthracis by using monoclonal antibody to cell wall galactose-N-acetylglucosamine polysaccharide. J. Clin. Microbiol 28:223–31 [Google Scholar]
  39. Fagan RP, Fairweather NF. 39.  2014. Biogenesis and functions of bacterial S-layers. Nat. Rev. Microbiol. 12:211–22 [Google Scholar]
  40. Farha MA, Leung A, Sewell EW, D'Elia MA, Allison SE. 40.  et al. 2013. Inhibition of WTA synthesis blocks the cooperative action of PBPs and sensitizes MRSA to β-lactams. ACS Chem. Biol. 8:226–33 [Google Scholar]
  41. Fieldhouse RJ, Turgeon Z, White D, Merrill AR. 41.  2010. Cholera- and anthrax-like toxins are among several new ADP-ribosyltransferases. PLOS Comput. Biol. 6:e1001029 [Google Scholar]
  42. Fischetti VA. 42.  2010. Bacteriophage endolysins: a novel anti-infective to control gram-positive pathogens. Int. J. Med. Microbiol 300:357–62 [Google Scholar]
  43. Forsberg LS, Abshire TG, Friedlander A, Quinn CP, Kannenberg EL, Carlson RW. 43.  2012. Localization and structural analysis of a conserved pyruvylated epitope in Bacillus anthracis secondary cell wall polysaccharides and characterization of the galactose deficient wall polysaccharide from avirulent B. anthracis CDC 684. Glycobiology 22:1103–17 [Google Scholar]
  44. Forsberg LS, Choudhury B, Leoff C, Marston CK, Hoffmaster AR. 44.  et al. 2011. Secondary cell wall polysaccharides from Bacilluscereus strains G9241, 03BB87 and 03BB102 causing fatal pneumonia share similar glycosyl structures with the polysaccharides from Bacillus anthracis. Glycobiology 21:934–48 [Google Scholar]
  45. Fouet A. 45.  2010. AtxA, a Bacillus anthracis global virulence regulator. Res. Microbiol. 161:735–42 [Google Scholar]
  46. Ganguly J, Low LY, Kamal N, Saile E, Forsberg LS. 46.  et al. 2013. The secondary cell wall polysaccharide of Bacillus anthracis provides the specific binding ligand for the C-terminal cell wall-binding domain of two phage endolysins, PlyL and PlyG. Glycobiology 23:820–32 [Google Scholar]
  47. Garufi G, Hendrickx AP, Beeri K, Kern JW, Sharma A. 47.  et al. 2012. Synthesis of lipoteichoic acids in Bacillus anthracis. J. Bacteriol. 194:4312–21 [Google Scholar]
  48. Ginsberg C, Zhang YH, Yuan Y, Walker S. 48.  2006. In vitro reconstitution of two essential steps in wall teichoic acid biosynthesis. ACS Chem. Biol. 1:25–28 [Google Scholar]
  49. Gordon VM, Klimpel KR, Arora N, Henderson MA, Leppla SH. 49.  1995. Proteolytic activation of bacterial toxins by eukaryotic cells is performed by furin and by additional cellular proteases. Infect. Immun. 63:82–87 [Google Scholar]
  50. Green BD, Battisti L, Koehler TM, Thorne CB, Ivins BE. 50.  1985. Demonstration of a capsule plasmid in Bacillus anthracis. Infect. Immun. 49:291–97 [Google Scholar]
  51. Guignot J, Mock M, Fouet A. 51.  1997. AtxA activates the transcription of genes harbored by both Bacillus anthracis virulence plasmids. FEMS Microbiol. Lett. 147:203–7 [Google Scholar]
  52. Hancock IC, Wiseman G, Baddiley J. 52.  1976. Biosynthesis of the unit that links teichoic acid to the bacterial wall: inhibition by tunicamycin. FEBS Lett 69:75–80 [Google Scholar]
  53. Helgason E, Økstad OA, Caugant DA, Johansen HA, Fouet A. 53.  et al. 2000. Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis—one species on the basis of genetic evidence. Appl. Environ. Microbiol 66:2627–30 [Google Scholar]
  54. Hoffmaster AR, Hill KK, Gee JE, Marston CK, De BK. 54.  et al. 2006. Characterization of Bacillus cereus isolates associated with fatal pneumonias: strains are closely related to Bacillusanthracis and harbor B. anthracis virulence genes. J. Clin. Microbiol 44:3352–60 [Google Scholar]
  55. Hoffmaster AR, Ravel J, Rasko DA, Chapman GD, Chute MD. 55.  et al. 2004. Identification of anthrax toxin genes in a Bacillus cereus associated with an illness resembling inhalation anthrax. PNAS 101:8449–54 [Google Scholar]
  56. Jensen GB, Hensen BM, Eilenberg J, Mahillon J. 56.  2003. The hidden lifestyles of Bacillus cereus and relatives. Environ. Microbiol. 5:631–40 [Google Scholar]
  57. Kaminska PS, Yernazarova A, Drewnowska JM, Zambrowski G, Swiecicka I. 57.  2015. The worldwide distribution of genetically and phylogenetically diverse Bacillus cereus isolates harbouring Bacillus anthracis-like plasmids. Environ. Microbiol. Rep 7:738–45 [Google Scholar]
  58. Kawai Y, Marles-Wright J, Cleverley RM, Emmins R, Ishikawa S. 58.  et al. 2011. A widespread family of bacterial cell wall assembly proteins. EMBO J 30:4931–41 [Google Scholar]
  59. Kaya S, Yokoyama K, Araki Y, Ito E. 59.  1984. N-acetylmannosaminyl(1–4)N-acetylglucosamine, a linkage unit between glycerol teichoic acid and peptidoglycan in cell walls of several Bacillus strains. J. Bacteriol 158:990–96 [Google Scholar]
  60. Keim PS, Wagner DM. 60.  2009. Humans and evolutionary and ecological forces shaped the phylogeography of recently emerged diseases. Nat. Rev. Microbiol. 7:813–21 [Google Scholar]
  61. Kern J, Ryan C, Faull K, Schneewind O. 61.  2010. Bacillus anthracis surface-layer proteins assemble by binding to the secondary cell wall polysaccharide in a manner that requires csaB and tagO. J. Mol. Biol 401:757–75 [Google Scholar]
  62. Kern JW, Schneewind O. 62.  2008. BslA, a pXO1-encoded adhesin of Bacillus anthracis. Mol. Microbiol. 68:504–15 [Google Scholar]
  63. Kern JW, Wilton R, Zhang R, Binkowski A, Joachimiak A, Schneewind O. 63.  2011. Structure of the SLH domains from Bacillus anthracis surface array protein. J. Biol. Chem. 286:26042–49 [Google Scholar]
  64. Kern VJ, Kern JW, Theriot JA, Schneewind O, Missiakas DM. 64.  2012. Surface (S)-layer proteins Sap and EA1 govern the binding of the S-layer associated protein BslO at the cell septa of Bacillus anthracis. J. Bacteriol. 194:3833–40 [Google Scholar]
  65. Kintzer AF, Thoren KL, Sterling HJ, Dong KC, Feld GK. 65.  et al. 2009. The protective antigen component of anthrax toxin forms functional octameric complexes. J. Mol. Biol. 392:614–29 [Google Scholar]
  66. Klee SR, Brzuszkiewicz EB, Nattermann H, Brüggemann H, Dupke S. 66.  et al. 2010. The genome of a Bacillus isolate causing anthrax in chimpanzees combines chromosomal properties of B. cereus with B. anthracis virulence plasmids. PLOS ONE 5:e10986 [Google Scholar]
  67. Klee SR, Ozel M, Appel B, Boesch C, Ellerbrok H. 67.  et al. 2006. Characterization of Bacillus anthracis-like bacteria isolated from wild great apes from Cote d'Ivoire and Cameroon. J. Bacteriol. 188:5333–44 [Google Scholar]
  68. Koch R. 68.  1876. Die Ätiologie der Milzbrand-Krankheit, begründet auf die Entwicklungsgeschichte des Bacillus anthracis. Beitr. Biol. Pflanz. 2:277–310 [Google Scholar]
  69. Koehler TM, Dai Z, Kaufman-Yarbray M. 69.  1994. Regulation of the Bacillus anthracis protective antigen gene: CO2 and a trans-acting element activate transcription from one of two promoters. J. Bacteriol 176:586–95 [Google Scholar]
  70. Kojima N, Araki Y, Ito E. 70.  1983. Structure of linkage region between ribitol teichoic acid and peptidoglycan in cell walls of Staphylococcus aureus H. J. Biol. Chem. 258:9043–45 [Google Scholar]
  71. Kojima N, Arakai Y, Ito E. 71.  1985. Structure of the linkage units between ribitol teichoic acids and peptidoglycan. J. Bacteriol. 161:299–306 [Google Scholar]
  72. Kolstø AB, Tourasse NJ, Økstad OA. 72.  2009. What sets Bacillus anthracis apart from other Bacillus species?. Annu. Rev. Microbiol 63:451–76 [Google Scholar]
  73. Krantz BA, Melnyk RA, Zhang S, Juris SJ, Lacy DB. 73.  et al. 2005. A phenylalanine clamp catalyzes protein translocation through the anthrax toxin pore. Science 309:777–81 [Google Scholar]
  74. Lazarevic V, Abellan FX, Möller SB, Karamata D, Mauël C. 74.  2002. Comparison of ribitol and glycerol teichoic acid genes in Bacillus subtilis W23 and 168: identical function, similar divergent organization, but different regulation. Microbiology 148:815–24 [Google Scholar]
  75. Leoff C, Choudhury B, Saile E, Quinn CP, Carlson RW, Kannenberg EL. 75.  2008. Structural elucidation of the non-classical secondary cell wall polysaccharide from Bacillus cereus ATCC 10987: Comparison with the polysaccharide from Bacillus anthracis and B. cereus type strain ATCC 14579 reveals both unique and common structural features. J. Biol. Chem 283:29812–21 [Google Scholar]
  76. Leppla SH. 76.  1982. Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclin AMP concentrations in eukaryotic cells. PNAS 79:3162–66 [Google Scholar]
  77. Levinsohn JL, Newman ZL, Hellmich KA, Fattah R, Getz MA. 77.  et al. 2012. Anthrax lethal factor cleavage of Nlrp1 is required for activation of the inflammasome. PLOS Pathog 8:e1002638 [Google Scholar]
  78. Lill R, Dowhan W, Wickner W. 78.  1990. The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins. Cell 60:271–80 [Google Scholar]
  79. Liszewski Zilla M, Chan YG, Lunderberg JM, Schneewind O, Missiakas D. 79.  2015. LytR-CpsA-Psr enzymes as determinants of Bacillus anthracis secondary cell wall polysaccharide assembly. J. Bacteriol. 197:343–53 [Google Scholar]
  80. Liszewski Zilla M, Lunderberg JM, Schneewind O, Missiakas D. 80.  2015. Bacillus anthracis lcp genes support vegetative growth, envelope assembly and spore formation. J. Bacteriol. 197:3731–41 [Google Scholar]
  81. Low LY, Yang C, Perego M, Osterman A, Liddington RC. 81.  2005. Structure and lytic activity of a Bacillus anthracis prophage endolysin. J. Biol. Chem. 280:35433–39 [Google Scholar]
  82. Lunderberg JM, Liszewski Zilla M, Missiakas D, Schneewind O. 82.  2015. Bacillus anthracis tagO is required for vegetative growth and secondary cell wall polysaccharide synthesis. J. Bacteriol. 197:3731–41 [Google Scholar]
  83. Lunderberg JM, Nguyen-Mau SM, Richter GS, Wang YT, Dworkin J. 83.  et al. 2013. Bacillus anthracis acetyltransferases PatA1 and PatA2 modify the secondary cell wall polysaccharide and affect the assembly of S-layer proteins. J. Bacteriol. 195:977–89 [Google Scholar]
  84. Maresso AW, Chapa TJ, Schneewind O. 84.  2006. Surface protein IsdC and sortase B are required for heme-iron scavenging of Bacillus anthracis. J. Bacteriol. 188:8145–52 [Google Scholar]
  85. Maresso AW, Garufi G, Schneewind O. 85.  2008. Bacillus anthracis secretes proteins that mediate heme acquisition from hemoglobin. PLOS Pathog 4:e1000132 [Google Scholar]
  86. Marston CK, Ibrahim H, Lee P, Churchwell G, Gumke M. 86.  et al. 2016. Anthrax toxin-expressing Bacillus cereus isolated from an anthrax-like eschar. PLOS ONE 11:e0156987 [Google Scholar]
  87. Mavroidi A, Aanensen DM, Godoy D, Skovsted IC, Kaltoft MS. 87.  et al. 2007. Genetic relatedness of the Streptococcus pneumoniae capsular biosynthetic loci. J. Bacteriol. 189:7841–55 [Google Scholar]
  88. Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P. 88.  et al. 2003. Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299:906–9 [Google Scholar]
  89. Mesnage S, Fontaine T, Mignot T, Delepierre M, Mock M, Fouet A. 89.  2000. Bacterial SLH domain proteins are non-covalently anchored to the cell surface via a conserved mechanism involving wall polysaccharide pyruvylation. EMBO J 19:4473–84 [Google Scholar]
  90. Mesnage S, Fouet A. 90.  2002. Plasmid-encoded autolysin in Bacillus anthracis: modular structure and catalytic properties. J. Bacteriol. 184:331–34 [Google Scholar]
  91. Mesnage S, Tosi-Couture E, Gounon P, Mock M, Fouet A. 91.  1998. The capsule and S-layer: two independent and yet compatible macromolecular structures in Bacillus anthracis. J. Bacteriol. 180:52–58 [Google Scholar]
  92. Mesnage S, Tosi-Couture E, Mock M, Fouet A. 92.  1999. The S-layer homology domain as a means for anchoring heterologous proteins on the cell surface of Bacillus anthracis. J. Appl. Microbiol. 87:256–60 [Google Scholar]
  93. Mesnage S, Tosi-Couture E, Mock M, Gounon P, Fouet A. 93.  1997. Molecular characterization of the Bacillus anthracis main S-layer component: evidence that it is the major cell-associated antigen. Mol. Microbiol. 23:1147–55 [Google Scholar]
  94. Mignot T, Couture-Tosi E, Mesnage S, Mock M, Fouet A. 94.  2004. In vivo Bacillus anthracis gene expression requires PagR as an intermediate effector of the AtxA signalling cascade. Int. J. Med. Microbiol 293:619–24 [Google Scholar]
  95. Mignot T, Mock M, Fouet A. 95.  2003. A plasmid-encoded regulator couples the synthesis of toxins and surface structures in Bacillus anthracis. Mol. Microbiol. 47:917–27 [Google Scholar]
  96. Mignot T, Mock M, Robichon D, Landier A, Lereclus D, Fouet A. 96.  2001. The incompatibility between the PlcR- and AtxA-controlled regulons may have selected a nonsense mutation in Bacillus anthracis. Mol. Microbiol. 42:1189–98 [Google Scholar]
  97. Milne J, Furlong D, Hanna PC, Wall JS, Collier RJ. 97.  1994. Anthrax protective antigen forms oligomers during intoxication of mammalian cells. J. Biol. Chem. 269:20607–12 [Google Scholar]
  98. Milne JC, Blanke SR, Hanna PC, Collier RJ. 98.  1995. Protective antigen-binding domain of anthrax lethal factor mediates translocation of a heterologous protein fused to its amino- or carboxy-terminus. Mol. Microbiol. 15:661–66 [Google Scholar]
  99. Mo KF, Li X, Li H, Low LY, Quinn CP, Boons GJ. 99.  2012. Endolysins of Bacillus anthracis bacteriophages recognize unique carbohydrate epitopes of vegetative cell wall polysaccharides with high affinity and selectivity. J. Am. Chem. Soc. 134:15556–62 [Google Scholar]
  100. Moayeri M, Leppla SH, Vrentas C, Pomerantsev AP, Liu S. 100.  2015. Anthrax pathogenesis. Annu. Rev. Microbiol. 69:185–208 [Google Scholar]
  101. Molnár J, Prágai B. 101.  1971. Attempts to detect the presence of teichoic acid in Bacillus anthracis. Acta Microbiol. Acad. Sci. Hung. 18:105–8 [Google Scholar]
  102. Nguyen-Mau S-M, Oh S-Y, Kern V, Missiakas D, Schneewind O. 102.  2012. Secretion genes as determinants of Bacillus anthracis chain length. J. Bacteriol. 194:3841–50 [Google Scholar]
  103. Nguyen-Mau S-M, Oh S-Y, Schneewind DI, Missiakas D, Schneewind O. 103.  2015. Bacillus anthracis SlaQ promotes S-layer protein assembly. J. Bacteriol. 197:3216–17 [Google Scholar]
  104. Oh S-Y, Budzik JM, Garufi G, Schneewind O. 104.  2011. Two capsular polysaccharides enable Bacillus cereus G9241 to cause anthrax-like disease. Mol. Microbiol. 79:455–70 [Google Scholar]
  105. Oh S-Y, Lunderberg JM, Chateau A, Schneewind O, Missiakas D. 105.  2016. Genes required for Bacillus anthracis secondary cell wall polysaccharide synthesis. J. Bacteriol. 199:e00613–16 [Google Scholar]
  106. Oh S-Y, Richter SG, Missiakas DM, Schneewind O. 106.  2015. Glutamate racemase mutants of Bacillus anthracis. J. Bacteriol. 197:1854–61 [Google Scholar]
  107. Okinaka R, Cloud K, Hampton O, Hoffmaster A, Hill K. 107.  et al. 1999. Sequence, assembly and analysis of pX01 and pX02. J. Appl. Microbiol. 87:261–62 [Google Scholar]
  108. Okinaka RT, Price EP, Wolken SR, Gruendike JM, Chung WK. 108.  et al. 2011. An attenuated strain of Bacillus anthracis (CDC 684) has a large chromosomal inversion and altered growth kinetics. BMC Genom 12:477–90 [Google Scholar]
  109. Oliver DB, Beckwith J. 109.  1981. E. coli mutant pleiotropically defective in the export of secreted proteins. Cell 25:765–72 [Google Scholar]
  110. Plaut RD, Beaber JW, Zemansky J, Kaur AP, George M. 110.  et al. 2014. Genetic evidence for the involvement of the S-layer protein gene sap and the sporulation genes spo0A, spo0B, and spo0F in phage AP50c infection of Bacillus anthracis. J. Bacteriol 196:1143–54 [Google Scholar]
  111. Preisz H. 111.  1909. Experimentelle Studien über Virulenz, Empfänglichkeit und Immunität beim Milzbrand. Z. Immunitäts-Forsch. 5:341–452 [Google Scholar]
  112. Priest FG, Barker M, Baillie LW, Holmes EC, Maiden MC. 112.  2004. Population structure and evolution of the Bacillus cereus group. J. Bacteriol. 186:7959–70 [Google Scholar]
  113. Pum D, Toca-Herrera JL, Sleytr UB. 113.  2013. S-layer protein self-assembly. Int. J. Mol. Sci. 14:2484–501 [Google Scholar]
  114. Rasko DA, Altherr MR, Han CS, Ravel J. 114.  2005. Genomics of the Bacillus cereus group of organisms. FEMS Microbiol. Rev. 29:303–29 [Google Scholar]
  115. Rasko DA, Rosovitz MJ, Økstad OA, Fouts DE, Jiang L. 115.  et al. 2007. Complete sequence analysis of novel plasmids from emetic and periodontal Bacillus cereus isolates reveals a common evolutionary history among the B. cereus-group plasmids, including Bacillus anthracis pXO1. J. Bacteriol 189:52–64 [Google Scholar]
  116. Read TD, Peterson SN, Tourasse N, Baille LW, Paulsen IT. 116.  et al. 2003. The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature 423:81–86 [Google Scholar]
  117. Reniere ML, Ukpabi GN, Harry SR, Stec DF, Krull R. 117.  et al. 2010. The IsdG-family of haem oxygenases degrades haem to a novel chromophore. Mol. Microbiol. 75:1529–38 [Google Scholar]
  118. Richter GS, Anderson VJ, Garufi G, Lu L, Joachimiak A. 118.  et al. 2009. Capsule anchoring in Bacillus anthracis occurs by a transpeptidation mechanism that is inhibited by capsidin. Mol. Microbiol. 71:404–20 [Google Scholar]
  119. Ristroph JD, Ivins BE. 119.  1983. Elaboration of Bacillus anthracis antigens in a new, defined culture medium. Infect. Immun. 39:483–86 [Google Scholar]
  120. Robertson DL, Leppla SH. 120.  1986. Molecular cloning and expression in Escherichia coli of the lethal factor gene of Bacillus anthracis. Gene 44:71–78 [Google Scholar]
  121. Rubinchik E, Schneider T, Elliott M, Scott WR, Pan J. 121.  et al. 2011. Mechanism of action and limited cross-resistance of new lipopeptide MX-2401. Antimicrob. Agents Chemother. 55:2743–54 [Google Scholar]
  122. Ruthel G, Ribot WJ, Bavari S, Hoover T. 122.  2004. Time-lapse confocal imaging of development of Bacillus anthracis in macrophages. J. Infect. Dis. 189:1313–16 [Google Scholar]
  123. Samuelson JC, Chen M, Jiang F, Moller I, Wiedmann M. 123.  et al. 2000. YidC mediates membrane protein insertion in bacteria. Nature 406:637–41 [Google Scholar]
  124. Sára M, Sleytr UB. 124.  2000. S-layer proteins. J. Bacteriol. 182:859–68 [Google Scholar]
  125. Scarff JM, Raynor MJ, Seldina YI, Ventura CL, Koehler TM, O'Brien AD. 125.  2016. The roles of AtxA orthologs in virulence of anthrax-like Bacillus cereus G9241. Mol. Microbiol. 102:545–61 [Google Scholar]
  126. Schneewind O, Missiakas DM. 126.  2012. Protein secretion and surface display in gram-positive bacteria. Philos. Trans. R. Soc. Lond. B 367:1123–39 [Google Scholar]
  127. Schuch R, Nelson D, Fischetti VA. 127.  2002. A bacteriolytic agent that detects and kills Bacillus anthracis. Nature 418:884–89 [Google Scholar]
  128. Schuch R, Pelzek AJ, Raz A, Euler CW, Ryan PA. 128.  et al. 2013. Use of a bacteriophage lysin to identify a novel target for antimicrobial development. PLOS ONE 8:e60754 [Google Scholar]
  129. Schulze RJ, Komar J, Botte M, Allen WJ, Whitehouse S. 129.  et al. 2014. Membrane protein insertion and proton-motive-force-dependent secretion through the bacterial holo-translocon SecYEG-SecDF-YajC-YidC. PNAS 111:4844–99 [Google Scholar]
  130. Scobie HM, Rainey GJ, Bradley KA, Young JA. 130.  2003. Human capillary morphogenesis protein 2 functions as an anthrax toxin receptor. PNAS 100:5170–74 [Google Scholar]
  131. Simon NC, Barbieri JT. 131.  2014. Bacillus cereus Certhrax ADP-ribosylates vinculin to disrupt focal adhesion complexes and cell adhesion. J. Biol. Chem. 289:10650–59 [Google Scholar]
  132. Skaar EP, Gaspar AH, Schneewind O. 132.  2006. Bacillus anthracis IsdG, a heme degrading monooxygenase. J. Bacteriol. 188:1071–80 [Google Scholar]
  133. Sleytr UB. 133.  1997. Basic and applied S-layer research: an overview. FEMS Microbiol. Rev. 20:5–12 [Google Scholar]
  134. Soldo B, Lazarevic V, Karamata D. 134.  2002. tagO is involved in the synthesis of all anionic cell-wall polymers in Bacillus subtilis 168. Microbiology 148:2079–87 [Google Scholar]
  135. Steichen C, Chen P, Kearney JF, Turnbough CLJ. 135.  2003. Identification of the immunodominant protein and other proteins of the Bacillus anthracis exosporium. J. Bacteriol. 185:1903–10 [Google Scholar]
  136. Tarlovsky Y, Fabian M, Solomaha E, Honsa E, Olson JS, Maresso AW. 136.  2010. A Bacillus anthracis S-layer homology protein that binds heme and mediates heme delivery to IsdC. J. Bacteriol. 192:3503–11 [Google Scholar]
  137. Tourasse NJ, Helgason E, Økstad OA, Hegna IK, Kolstø AB. 137.  2006. The Bacillus cereus group: novel aspects of population structure and genome dynamics. J. Appl. Microbiol. 101:579–93 [Google Scholar]
  138. Tsirigotaki A, De Geyter J, Šoštaric N, Economou A, Karamanou S. 138.  2017. Protein export through the bacterial Sec pathway. Nat. Rev. Microbiol. 15:21–36 [Google Scholar]
  139. Turnbull PC. 139.  1999. Definitive identification of Bacillus anthracis—a review. J. Appl. Microbiol. 87:237–40 [Google Scholar]
  140. Turnbull PC. 140.  2002. Introduction: anthrax history, disease and ecology. Curr. Top. Microbiol. Immunol. 271:1–19 [Google Scholar]
  141. Uchida I, Hornung JM, Thorne CB, Klimpel KR, Leppla SH. 141.  1993. Cloning and characterization of a gene whose product is a trans-activator of anthrax toxin synthesis. J. Bacteriol. 175:5329–38 [Google Scholar]
  142. Uchida I, Makino S, Sekizaki T, Terakado N. 142.  1997. Cross-talk to the genes for Bacillus anthracis capsule synthesis by atxA, the gene encoding the trans-activator of anthrax toxin synthesis. Mol. Microbiol 23:1229–40 [Google Scholar]
  143. Visschedyk D, Rochon A, Tempel W, Dimov S, Park HW, Merrill AR. 143.  2012. Certhrax toxin, an anthrax-related ADP-ribosyltransferase from Bacillus cereus. J. Biol. Chem. 287:41089–102 [Google Scholar]
  144. Vodkin MH, Leppla SH. 144.  1983. Cloning of the protective antigen gene of Bacillus anthracis. Cell 34:693–97 [Google Scholar]
  145. Wang Y, Wei Y, Yuan S, Tao H, Dong J. 145.  et al. 2016. Bacillus anthracis S-layer protein BslA binds to extracellular matrix by interacting with laminin. BMC Microbiol 16:183 [Google Scholar]
  146. Wang YT, Missiakas D, Schneewind O. 146.  2014. GneZ, a UDP-GlcNAc 2-epimerase, is required for S-layer assembly and vegetative growth of Bacillus anthracis. J. Bacteriol. 196:2969–78 [Google Scholar]
  147. Wang YT, Oh SY, Hendrickx AP, Lunderberg JM, Schneewind O. 147.  2013. Bacillus cereus G9241 S-layer assembly contributes to the pathogenesis of anthrax-like disease in mice. J. Bacteriol. 195:596–605 [Google Scholar]
  148. Weidenmaier C, Kokai-Kun JF, Kristian SA, Chanturiya T, Kalbacher H. 148.  et al. 2004. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat. Med. 10:243–45 [Google Scholar]
  149. Wright AM, Beres SB, Consamus EN, Long SW, Flores AR. 149.  et al. 2011. Rapidly progressive, fatal, inhalation anthrax-like infection in a human: case report, pathogen genome sequencing, pathology, and coordinated response. Arch. Pathol. Lab. Med. 135:1447–59 [Google Scholar]
  150. Yother J. 150.  2011. Capsules of Streptococcus pneumoniae and other bacteria: paradigms for polysaccharide biosynthesis and regulation. Annu. Rev. Microbiol. 65:563–81 [Google Scholar]
  151. Zhao J, Milne JC, Collier RJ. 151.  1995. Effect of anthrax toxin's lethal factor on ion channels formed by the protective antigen. J. Biol. Chem. 270:18626–30 [Google Scholar]
  152. Zwick ME, Joseph SJ, Didelot X, Chen PE, Bishop-Lilly KA. 152.  et al. 2012. Genomic characterization of the Bacillus cereus sensu lato species: backdrop to the evolution of Bacillus anthracis. Genome Res 22:1512–24 [Google Scholar]
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