1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

The Group: Species with Pathogenic Potential

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Buy this Microbiology Spectrum Article
Price Non-Member $15.00
  • Authors: Monika Ehling-Schulz1, Didier Lereclus2, Theresa M. Koehler3
  • Editors: Vincent A. Fischetti4, Richard P. Novick5, Joseph J. Ferretti6, Daniel A. Portnoy7, Miriam Braunstein8, Julian I. Rood9
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Institute of Microbiology, Department of Pathology, University of Veterinary Medicine, 1210 Vienna, Austria; 2: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, 78350 Jouy-en-Josas, France; 3: Department of Microbiology and Molecular Genetics, McGovern Medical School, University of Texas Health Science Center – Houston, Houston, TX 77030; 4: The Rockefeller University, New York, NY; 5: Skirball Institute for Molecular Medicine, NYU Medical Center, New York, NY; 6: Department of Microbiology & Immunology, University of Oklahoma Health Science Center, Oklahoma City, OK; 7: Department of Molecular and Cellular Microbiology, University of California, Berkeley, Berkeley, CA; 8: Department of Microbiology and Immunology, University of North Carolina-Chapel Hill, Chapel Hill, NC; 9: Infection and Immunity Program, Monash Biomedicine Discovery Institute, Monash University, Melbourne, Australia
  • Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0032-2018
  • Received 08 May 2018 Accepted 29 September 2018 Published 17 May 2019
  • Theresa M. Koehler, [email protected]
image of The <span class="jp-italic">Bacillus cereus</span> Group: <span class="jp-italic">Bacillus</span> Species with Pathogenic Potential
    Preview this microbiology spectrum article:
    Zoom in
    Zoomout

    The Group: Species with Pathogenic Potential, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/7/3/GPP3-0032-2018-1.gif /docserver/preview/fulltext/microbiolspec/7/3/GPP3-0032-2018-2.gif
  • Abstract:

    The group includes several species with closely related phylogeny. The most well-studied members of the group, , , and , are known for their pathogenic potential. Here, we present the historical rationale for speciation and discuss shared and unique features of these bacteria. Aspects of cell morphology and physiology, and genome sequence similarity and gene synteny support close evolutionary relationships for these three species. For many strains, distinct differences in virulence factor synthesis provide facile means for species assignment. is the causative agent of anthrax. Some strains are commonly recognized as food poisoning agents, but strains can also cause localized wound and eye infections as well as systemic disease. Certain strains are entomopathogens and have been commercialized for use as biopesticides, while some strains have been reported to cause infection in immunocompromised individuals. In this article we compare and contrast , , and , including ecology, cell structure and development, virulence attributes, gene regulation and genetic exchange systems, and experimental models of disease.

  • Citation: Ehling-Schulz M, Lereclus D, Koehler T. 2019. The Group: Species with Pathogenic Potential. Microbiol Spectrum 7(3):GPP3-0032-2018. doi:10.1128/microbiolspec.GPP3-0032-2018.

References

1. Liu Y, Lai Q, Göker M, Meier-Kolthoff JP, Wang M, Sun Y, Wang L, Shao Z. 2015. Genomic insights into the taxonomic status of the Bacillus cereus group. Sci Rep 5:14082 http://dx.doi.org/10.1038/srep14082. [PubMed]
2. Lapidus A, Goltsman E, Auger S, Galleron N, Ségurens B, Dossat C, Land ML, Broussolle V, Brillard J, Guinebretiere MH, Sanchis V, Nguen-The C, Lereclus D, Richardson P, Wincker P, Weissenbach J, Ehrlich SD, Sorokin A. 2008. Extending the Bacillus cereus group genomics to putative food-borne pathogens of different toxicity. Chem Biol Interact 171:236–249 http://dx.doi.org/10.1016/j.cbi.2007.03.003. [PubMed]
3. Kolstø AB, Lereclus D, Mock M. 2002. Genome structure and evolution of the Bacillus cereus group. Curr Top Microbiol Immunol 264:95–108.
4. Rasko DA, Altherr MR, Han CS, Ravel J. 2005. Genomics of the Bacillus cereus group of organisms. FEMS Microbiol Rev 29:303–329. [PubMed]
5. Okinaka R, Cloud K, Hampton O, Hoffmaster A, Hill K, Keim P, Koehler T, Lamke G, Kumano S, Manter D, Martinez Y, Ricke D, Svensson R, Jackson P. 1999. Sequence, assembly and analysis of pX01 and pX02. J Appl Microbiol 87:261–262 http://dx.doi.org/10.1046/j.1365-2672.1999.00883.x. [PubMed]
6. Ehling-Schulz M, Fricker M, Grallert H, Rieck P, Wagner M, Scherer S. 2006. Cereulide synthetase gene cluster from emetic Bacillus cereus: structure and location on a mega virulence plasmid related to Bacillus anthracis toxin plasmid pXO1. BMC Microbiol 6:20 http://dx.doi.org/10.1186/1471-2180-6-20. [PubMed]
7. Rasko DA, Rosovitz MJ, Økstad OA, Fouts DE, Jiang L, Cer RZ, Kolstø AB, Gill SR, Ravel J. 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 http://dx.doi.org/10.1128/JB.01313-06. [PubMed]
8. Lereclus D, Ribier J, Klier A, Menou G, Lecadet M-M. 1984. A transposon-like structure related to the delta-endotoxin gene of Bacillus thuringiensis. EMBO J 3:2561–2567 http://dx.doi.org/10.1002/j.1460-2075.1984.tb02174.x. [PubMed]
9. Berry C, O’Neil S, Ben-Dov E, Jones AF, Murphy L, Quail MA, Holden MT, Harris D, Zaritsky A, Parkhill J. 2002. Complete sequence and organization of pBtoxis, the toxin-coding plasmid of Bacillus thuringiensis subsp. israelensis. Appl Environ Microbiol 68:5082–5095 http://dx.doi.org/10.1128/AEM.68.10.5082-5095.2002. [PubMed]
10. Kronstad JW, Whiteley HR. 1984. Inverted repeat sequences flank a Bacillus thuringiensis crystal protein gene. J Bacteriol 160:95–102.
11. Di Franco C, Beccari E, Santini T, Pisaneschi G, Tecce G. 2002. Colony shape as a genetic trait in the pattern-forming Bacillus mycoides. BMC Microbiol 2:33 http://dx.doi.org/10.1186/1471-2180-2-33. [PubMed]
12. Nakamura LK. 1998. Bacillus pseudomycoides sp. nov. Int J Syst Bacteriol 48:1031–1035 http://dx.doi.org/10.1099/00207713-48-3-1031. [PubMed]
13. Lechner S, Mayr R, Francis KP, Prüss BM, Kaplan T, Wiessner-Gunkel E, Stewart GS, Scherer S. 1998. Bacillus weihenstephanensis sp. nov. is a new psychrotolerant species of the Bacillus cereus group. Int J Syst Bacteriol 48:1373–1382 http://dx.doi.org/10.1099/00207713-48-4-1373. [PubMed]
14. Guinebretière MH, Auger S, Galleron N, Contzen M, De Sarrau B, De Buyser ML, Lamberet G, Fagerlund A, Granum PE, Lereclus D, De Vos P, Nguyen-The C, Sorokin A. 2013. Bacillus cytotoxicus sp. nov. is a novel thermotolerant species of the Bacillus cereus group occasionally associated with food poisoning. Int J Syst Evol Microbiol 63:31–40 http://dx.doi.org/10.1099/ijs.0.030627-0. [PubMed]
15. Jiménez G, Urdiain M, Cifuentes A, López-López A, Blanch AR, Tamames J, Kämpfer P, Kolstø AB, Ramón D, Martínez JF, Codoñer FM, Rosselló-Móra R. 2013. Description of Bacillus toyonensis sp. nov., a novel species of the Bacillus cereus group, and pairwise genome comparisons of the species of the group by means of ANI calculations. Syst Appl Microbiol 36:383–391 http://dx.doi.org/10.1016/j.syapm.2013.04.008. [PubMed]
16. Helgason E, Økstad OA, Caugant DA, Johansen HA, Fouet A, Mock M, Hegna I, Kolstø AB. 2000. Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis: one species on the basis of genetic evidence. Appl Environ Microbiol 66:2627–2630 http://dx.doi.org/10.1128/AEM.66.6.2627-2630.2000. [PubMed]
17. Agaisse H, Gominet M, Økstad OA, Kolstø AB, Lereclus D. 1999. PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis. Mol Microbiol 32:1043–1053 http://dx.doi.org/10.1046/j.1365-2958.1999.01419.x. [PubMed]
18. Mignot T, Mock M, Robichon D, Landier A, Lereclus D, Fouet A. 2001. The incompatibility between the PlcR- and AtxA-controlled regulons may have selected a nonsense mutation in Bacillus anthracis. Mol Microbiol 42:1189–1198 http://dx.doi.org/10.1046/j.1365-2958.2001.02692.x.
19. Koch R. 1876. Die Ätiologie der Milzbrand-Krankheit, begründet auf die Entwicklungsgeschichte des Bacillus anthracis. Beitr Biol Pflanz 2:277–310.
20. Pasteur L. 1881. Le vaccin du charbon. C R Acad Sci 92:666–668.
21. Klee SR, Ozel M, Appel B, Boesch C, Ellerbrok H, Jacob D, Holland G, Leendertz FH, Pauli G, Grunow R, Nattermann H. 2006. Characterization of Bacillus anthracis-like bacteria isolated from wild great apes from Cote d’Ivoire and Cameroon. J Bacteriol 188:5333–5344 http://dx.doi.org/10.1128/JB.00303-06. [PubMed]
22. Brézillon C, Haustant M, Dupke S, Corre JP, Lander A, Franz T, Monot M, Couture-Tosi E, Jouvion G, Leendertz FH, Grunow R, Mock ME, Klee SR, Goossens PL. 2015. Capsules, toxins and AtxA as virulence factors of emerging Bacillus cereus biovar anthracis. PLoS Negl Trop Dis 9:e0003455 http://dx.doi.org/10.1371/journal.pntd.0003455. [PubMed]
23. Miller JM, Hair JG, Hebert M, Hebert L, Roberts FJ Jr, Weyant RS. 1997. Fulminating bacteremia and pneumonia due to Bacillus cereus. J Clin Microbiol 35:504–507.
24. Hoffmaster AR, Ravel J, Rasko DA, Chapman GD, Chute MD, Marston CK, De BK, Sacchi CT, Fitzgerald C, Mayer LW, Maiden MC, Priest FG, Barker M, Jiang L, Cer RZ, Rilstone J, Peterson SN, Weyant RS, Galloway DR, Read TD, Popovic T, Fraser CM. 2004. Identification of anthrax toxin genes in a Bacillus cereus associated with an illness resembling inhalation anthrax. Proc Natl Acad Sci U S A 101:8449–8454 http://dx.doi.org/10.1073/pnas.0402414101. [PubMed]
25. Avashia SB, Riggins WS, Lindley C, Hoffmaster A, Drumgoole R, Nekomoto T, Jackson PJ, Hill KK, Williams K, Lehman L, Libal MC, Wilkins PP, Alexander J, Tvaryanas A, Betz T. 2007. Fatal pneumonia among metalworkers due to inhalation exposure to Bacillus cereus containing Bacillus anthracis toxin genes. Clin Infect Dis 44:414–416 http://dx.doi.org/10.1086/510429. [PubMed]
26. Wright AM, Beres SB, Consamus EN, Long SW, Flores AR, Barrios R, Richter GS, Oh SY, Garufi G, Maier H, Drews AL, Stockbauer KE, Cernoch P, Schneewind O, Olsen RJ, Musser JM. 2011. Rapidly progressive, fatal, inhalation anthrax-like infection in a human: case report, pathogen genome sequencing, pathology, and coordinated response. Arch Pathol Lab Med 135:1447–1459 http://dx.doi.org/10.5858/2011-0362-SAIR.1. [PubMed]
27. Gee JE, Marston CK, Sammons SA, Burroughs MA, Hoffmaster AR. 2014. Draft genome sequence of Bacillus cereus strain BcFL2013, a clinical isolate similar to G9241. Genome Announc 2:e00469-14 http://dx.doi.org/10.1128/genomeA.00469-14. [PubMed]
28. Visschedyk D, Rochon A, Tempel W, Dimov S, Park HW, Merrill AR. 2012. Certhrax toxin, an anthrax-related ADP-ribosyltransferase from Bacillus cereus. J Biol Chem 287:41089–41102 http://dx.doi.org/10.1074/jbc.M112.412809. [PubMed]
29. Simon NC, Vergis JM, Ebrahimi AV, Ventura CL, O’Brien AD, Barbieri JT. 2013. Host cell cytotoxicity and cytoskeleton disruption by CerADPr, an ADP-ribosyltransferase of Bacillus cereus G9241. Biochemistry 52:2309–2318 http://dx.doi.org/10.1021/bi300692g. [PubMed]
30. Simon NC, Barbieri JT. 2014. Bacillus cereus Certhrax ADP-ribosylates vinculin to disrupt focal adhesion complexes and cell adhesion. J Biol Chem 289:10650–10659 http://dx.doi.org/10.1074/jbc.M113.500710. [PubMed]
31. Oh SY, Budzik JM, Garufi G, Schneewind O. 2011. Two capsular polysaccharides enable Bacillus cereus G9241 to cause anthrax-like disease. Mol Microbiol 80:455–470 http://dx.doi.org/10.1111/j.1365-2958.2011.07582.x. [PubMed]
32. Wilson MK, Vergis JM, Alem F, Palmer JR, Keane-Myers AM, Brahmbhatt TN, Ventura CL, O’Brien AD. 2011. Bacillus cereus G9241 makes anthrax toxin and capsule like highly virulent B. anthracis Ames but behaves like attenuated toxigenic nonencapsulated B. anthracis Sterne in rabbits and mice. Infect Immun 79:3012–3019 http://dx.doi.org/10.1128/IAI.00205-11. [PubMed]
33. Frankland GC, Frankland PF. 1887. Studies on some new micro-organisms obtained from air. R Soc Lond Philos Trans B 178:257–287 http://dx.doi.org/10.1098/rstb.1887.0011.
34. Bottone EJ. 2010. Bacillus cereus, a volatile human pathogen. Clin Microbiol Rev 23:382–398 http://dx.doi.org/10.1128/CMR.00073-09. [PubMed]
35. Ehling-Schulz M, Knutsson R, Scherer S. 2011. Bacillus cereus, p 147–164. In Kathariou S, Fratamico P, Lui Y (ed), Genomes of Food- and Water-Borne Pathogens. ASM Press, Washington DC.
36. Hauge S. 1955. Food poisoning caused by aerobic spore forming bacilli. J Appl Bacteriol 18:591–595 http://dx.doi.org/10.1111/j.1365-2672.1955.tb02116.x.
37. Stenfors Arnesen LP, Fagerlund A, Granum PE. 2008. From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 32:579–606 http://dx.doi.org/10.1111/j.1574-6976.2008.00112.x. [PubMed]
38. Fedhila S, Nel P, Lereclus D. 2002. The InhA2 metalloprotease of Bacillus thuringiensis strain 407 is required for pathogenicity in insects infected via the oral route. J Bacteriol 184:3296–3304 http://dx.doi.org/10.1128/JB.184.12.3296-3304.2002. [PubMed]
39. Doll VM, Ehling-Schulz M, Vogelmann R. 2013. Concerted action of sphingomyelinase and non-hemolytic enterotoxin in pathogenic Bacillus cereus. PLoS One 8:e61404 http://dx.doi.org/10.1371/journal.pone.0061404. [PubMed]
40. Böhm ME, Huptas C, Krey VM, Scherer S. 2015. Massive horizontal gene transfer, strictly vertical inheritance and ancient duplications differentially shape the evolution of Bacillus cereus enterotoxin operons hbl, cytK and nhe. BMC Evol Biol 15:246 http://dx.doi.org/10.1186/s12862-015-0529-4. [PubMed]
41. Ehling-Schulz M, Svensson B, Guinebretiere MH, Lindbäck T, Andersson M, Schulz A, Fricker M, Christiansson A, Granum PE, Märtlbauer E, Nguyen-The C, Salkinoja-Salonen M, Scherer S. 2005. Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains. Microbiology 151:183–197 http://dx.doi.org/10.1099/mic.0.27607-0. [PubMed]
42. Ehling-Schulz M, Vukov N, Schulz A, Shaheen R, Andersson M, Märtlbauer E, Scherer S. 2005. Identification and partial characterization of the nonribosomal peptide synthetase gene responsible for cereulide production in emetic Bacillus cereus. Appl Environ Microbiol 71:105–113 http://dx.doi.org/10.1128/AEM.71.1.105-113.2005. [PubMed]
43. Ishiwata I. 1901. On a kind of severe flacherie (sotto diseases). Dainihon Sanshi Kaiho 114:1–5.
44. Berliner E. 1915. Uber die Schlaffsucht der Mehlmottenraupe (Ephestia kuhniella, Zell.) ihren Erreger, Bacillus thuringiensisn. sp. Z Angew Entomol 2:29–56 http://dx.doi.org/10.1111/j.1439-0418.1915.tb00334.x.
45. Goldberg LH, Margalit J. 1977. A bacterial spore demonstrating rapid larvicidal activity against Anopheles sergentii, Uranotaenia unguiculata, Culex univitatus, Aedes aegypti and Culex pipiens. Mosq News 37:355–358.
46. Krieg A, Huger AM, Langenbruch GA, Schnetter W. 1983. Bacillus thuringiensis var. tenebrionis: ein neuer gegenuber arven von Coleopteren wirksamer athotyp. Z Ang Ent 96:500–508 http://dx.doi.org/10.1111/j.1439-0418.1983.tb03704.x.
47. Wei JZ, Hale K, Carta L, Platzer E, Wong C, Fang SC, Aroian RV. 2003. Bacillus thuringiensis crystal proteins that target nematodes. Proc Natl Acad Sci U S A 100:2760–2765 http://dx.doi.org/10.1073/pnas.0538072100. [PubMed]
48. Sanchis V. 2011. From microbial sprays to insect-resistant transgenic plants: history of the biospesticide Bacillus thuringiensis. A review. Agron Sustain Dev 31:217–231 http://dx.doi.org/10.1051/agro/2010027.
49. Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler DR, Dean DH. 1998. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62:775–806.
50. Espinasse S, Chaufaux J, Buisson C, Perchat S, Gohar M, Bourguet D, Sanchis V. 2003. Occurrence and linkage between secreted insecticidal toxins in natural isolates of Bacillus thuringiensis. Curr Microbiol 47:501–507 http://dx.doi.org/10.1007/s00284-003-4097-2. [PubMed]
51. González JMJ Jr, Brown BJ, Carlton BC. 1982. Transfer of Bacillus thuringiensis plasmids coding for delta-endotoxin among strains of B. thuringiensis and B. cereus. Proc Natl Acad Sci U S A 79:6951–6955 http://dx.doi.org/10.1073/pnas.79.22.6951. [PubMed]
52. Mahillon J, Rezsöhazy R, Hallet B, Delcour J. 1994. IS 231 and other Bacillus thuringiensis transposable elements: a review. Genetica 93:13–26 http://dx.doi.org/10.1007/BF01435236. [PubMed]
53. Menou G, Mahillon J, Lecadet MM, Lereclus D. 1990. Structural and genetic organization of IS 232, a new insertion sequence of Bacillus thuringiensis. J Bacteriol 172:6689–6696 http://dx.doi.org/10.1128/jb.172.12.6689-6696.1990. [PubMed]
54. Jensen GB, Hansen BM, Eilenberg J, Mahillon J. 2003. The hidden lifestyles of Bacillus cereus and relatives. Environ Microbiol 5:631–640 http://dx.doi.org/10.1046/j.1462-2920.2003.00461.x. [PubMed]
55. Martin PAW, Travers RS. 1989. Worldwide abundance and distribution of Bacillus thuringiensis isolates. Appl Environ Microbiol 55:2437–2442.
56. Meadows MP, Ellis DJ, Butt J, Jarrett P, Burges HD. 1992. Distribution, frequency, and diversity of Bacillus thuringiensis in an animal feed mill. Appl Environ Microbiol 58:1344–1350.
57. Smith RA, Couche GA. 1991. The phyllophane as a source of Bacillus thuringiensis variants. Appl Environ Microbiol 57:311–315.
58. Messelhäusser U, Frenzel E, Blöchinger C, Zucker R, Kämpf P, Ehling-Schulz M. 2014. Emetic Bacillus cereus are more volatile than thought: recent foodborne outbreaks and prevalence studies in Bavaria (2007-2013). BioMed Res Int 2014:465603 http://dx.doi.org/10.1155/2014/465603. [PubMed]
59. Hoton FM, Fornelos N, N’guessan E, Hu X, Swiecicka I, Dierick K, Jääskeläinen E, Salkinoja-Salonen M, Mahillon J. 2009. Family portrait of Bacillus cereus and Bacillus weihenstephanensis cereulide-producing strains. Environ Microbiol Rep 1:177–183 http://dx.doi.org/10.1111/j.1758-2229.2009.00028.x. [PubMed]
60. Monnerat RG, Soares CM, Capdeville G, Jones G, Martins ES, Praça L, Cordeiro BA, Braz SV, dos Santos RC, Berry C. 2009. Translocation and insecticidal activity of Bacillus thuringiensis living inside of plants. Microb Biotechnol 2:512–520 http://dx.doi.org/10.1111/j.1751-7915.2009.00116.x. [PubMed]
61. Vilas-Bôas LA, Vilas-Bôas GF, Saridakis HO, Lemos MV, Lereclus D, Arantes OM. 2000. Survival and conjugation of Bacillus thuringiensis in a soil microcosm. FEMS Microbiol Ecol 31:255–259 http://dx.doi.org/10.1016/S0168-6496(00)00002-7.
62. West AW, Burges HD, Dixon TJ, Wyborn CH. 1985. Survival of Bacillus thuringiensis and Bacillus cereus spore inocula in soil: effects of pH, moisture, nutrient availability and indigenous microorganisms. Soil Biol Biochem 17:657–665 http://dx.doi.org/10.1016/0038-0717(85)90043-4.
63. Saile E, Koehler TM. 2006. Bacillus anthracis multiplication, persistence, and genetic exchange in the rhizosphere of grass plants. Appl Environ Microbiol 72:3168–3174 http://dx.doi.org/10.1128/AEM.72.5.3168-3174.2006. [PubMed]
64. Fricker M, Ågren J, Segerman B, Knutsson R, Ehling-Schulz M. 2011. Evaluation of Bacillus strains as model systems for the work on Bacillus anthracis spores. Int J Food Microbiol 145(Suppl 1) :S129–S136 http://dx.doi.org/10.1016/j.ijfoodmicro.2010.07.036. [PubMed]
65. Hoornstra D, Andersson MA, Teplova VV, Mikkola R, Uotila LM, Andersson LC, Roivainen M, Gahmberg CG, Salkinoja-Salonen MS. 2013. Potato crop as a source of emetic Bacillus cereus and cereulide-induced mammalian cell toxicity. Appl Environ Microbiol 79:3534–3543 http://dx.doi.org/10.1128/AEM.00201-13. [PubMed]
66. Ehling-Schulz M, Frenzel E, Gohar M. 2015. Food-bacteria interplay: pathometabolism of emetic Bacillus cereus. Front Microbiol 6:704 http://dx.doi.org/10.3389/fmicb.2015.00704.
67. Halverson LJ, Clayton MK, Handelsman J. 1993. Variable stability of antibiotic-resistance markers in Bacillus cereus UW85 in the soybean rhizosphere in the field. Mol Ecol 2:65–78 http://dx.doi.org/10.1111/j.1365-294X.1993.tb00001.x. [PubMed]
68. Dutta S, Rani TS, Podile AR. 2013. Root exudate-induced alterations in Bacillus cereus cell wall contribute to root colonization and plant growth promotion. PLoS One 8:e78369 http://dx.doi.org/10.1371/journal.pone.0078369. [PubMed]
69. Wang S, Zheng Y, Gu C, He C, Yang M, Zhang X, Guo J, Zhao H, Niu D. 2017. Bacillus cereus AR156 activates defense responses to Pseudomonas syringae pv. tomato in Arabidopsis thaliana similarly to flg22. Mol Plant Microbe Interact 31:311–322. [PubMed]
70. Gohar M, Faegri K, Perchat S, Ravnum S, Økstad OA, Gominet M, Kolstø AB, Lereclus D. 2008. The PlcR virulence regulon of Bacillus cereus. PLoS One 3:e2793 http://dx.doi.org/10.1371/journal.pone.0002793. [PubMed]
71. Ivanova N, Sorokin A, Anderson I, Galleron N, Candelon B, Kapatral V, Bhattacharyya A, Reznik G, Mikhailova N, Lapidus A, Chu L, Mazur M, Goltsman E, Larsen N, D’Souza M, Walunas T, Grechkin Y, Pusch G, Haselkorn R, Fonstein M, Ehrlich SD, Overbeek R, Kyrpides N. 2003. Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423:87–91 http://dx.doi.org/10.1038/nature01582. [PubMed]
72. Raymond B, Johnston PR, Nielsen-LeRoux C, Lereclus D, Crickmore N. 2010. Bacillus thuringiensis: an impotent pathogen? Trends Microbiol 18:189–194 http://dx.doi.org/10.1016/j.tim.2010.02.006. [PubMed]
73. Braun P, Grass G, Aceti A, Serrecchia L, Affuso A, Marino L, Grimaldi S, Pagano S, Hanczaruk M, Georgi E, Northoff B, Schöler A, Schloter M, Antwerpen M, Fasanella A. 2015. Microevolution of anthrax from a young ancestor (M.A.Y.A.) suggests a soil-borne life cycle of Bacillus anthracis. PLoS One 10:e0135346 http://dx.doi.org/10.1371/journal.pone.0135346. [PubMed]
74. Antonation KS, Grützmacher K, Dupke S, Mabon P, Zimmermann F, Lankester F, Peller T, Feistner A, Todd A, Herbinger I, de Nys HM, Muyembe-Tamfun JJ, Karhemere S, Wittig RM, Couacy-Hymann E, Grunow R, Calvignac-Spencer S, Corbett CR, Klee SR, Leendertz FH. 2016. Bacillus cereus biovar anthracis causing anthrax in sub-Saharan Africa: chromosomal monophyly and broad geographic distribution. PLoS Negl Trop Dis 10:e0004923 http://dx.doi.org/10.1371/journal.pntd.0004923. [PubMed]
75. Scarff JM, Raynor MJ, Seldina YI, Ventura CL, Koehler TM, O’Brien AD. 2016. The roles of AtxA orthologs in virulence of anthrax-like Bacillus cereus G9241. Mol Microbiol 102:545–561 http://dx.doi.org/10.1111/mmi.13478. [PubMed]
76. Argôlo-Filho RC, Loguercio LL. 2013. Bacillus thuringiensis is an environmental pathogen and host-specificity has developed as an adaptation to human-generated ecological niches. Insects 5:62–91 http://dx.doi.org/10.3390/insects5010062. [PubMed]
77. Blackburn JK, Matakarimov S, Kozhokeeva S, Tagaeva Z, Bell LK, Kracalik IT, Zhunushov A. 2017. Modeling the ecological niche of Bacillus anthracis to map anthrax risk in Kyrgyzstan. Am J Trop Med Hyg 96:550–556. [PubMed]
78. Hugh-Jones M, Blackburn J. 2009. The ecology of Bacillus anthracis. Mol Aspects Med 30:356–367 http://dx.doi.org/10.1016/j.mam.2009.08.003. [PubMed]
79. Valseth K, Nesbø CL, Easterday WR, Turner WC, Olsen JS, Stenseth NC, Haverkamp THA. 2017. Temporal dynamics in microbial soil communities at anthrax carcass sites. BMC Microbiol 17:206 http://dx.doi.org/10.1186/s12866-017-1111-6. [PubMed]
80. Dey R, Hoffman PS, Glomski IJ. 2012. Germination and amplification of anthrax spores by soil-dwelling amoebas. Appl Environ Microbiol 78:8075–8081 http://dx.doi.org/10.1128/AEM.02034-12. [PubMed]
81. Barandongo ZR, Mfune JKE, Turner WC. 2017. Dust-bathing behaviors of African herbivores and the potential risk of inhalational anthrax. J Wildl Dis 54:34–44. [PubMed]
82. Turner WC, Kausrud KL, Beyer W, Easterday WR, Barandongo ZR, Blaschke E, Cloete CC, Lazak J, Van Ert MN, Ganz HH, Turnbull PC, Stenseth NC, Getz WM. 2016. Lethal exposure: an integrated approach to pathogen transmission via environmental reservoirs. Sci Rep 6:27311 http://dx.doi.org/10.1038/srep27311. [PubMed]
83. Turnbull PC. 2002. Introduction: anthrax history, disease and ecology. Curr Top Microbiol Immunol 271:1–19 http://dx.doi.org/10.1007/978-3-662-05767-4_1. [PubMed]
84. Jernigan DB, Raghunathan PL, Bell BP, Brechner R, Bresnitz EA, Butler JC, Cetron M, Cohen M, Doyle T, Fischer M, Greene C, Griffith KS, Guarner J, Hadler JL, Hayslett JA, Meyer R, Petersen LR, Phillips M, Pinner R, Popovic T, Quinn CP, Reefhuis J, Reissman D, Rosenstein N, Schuchat A, Shieh WJ, Siegal L, Swerdlow DL, Tenover FC, Traeger M, Ward JW, Weisfuse I, Wiersma S, Yeskey K, Zaki S, Ashford DA, Perkins BA, Ostroff S, Hughes J, Fleming D, Koplan JP, Gerberding JL, National Anthrax Epidemiologic Investigation Team. 2002. Investigation of bioterrorism-related anthrax, United States, 2001: epidemiologic findings. Emerg Infect Dis 8:1019–1028 http://dx.doi.org/10.3201/eid0810.020353. [PubMed]
85. Fouet A. 2009. The surface of Bacillus anthracis. Mol Aspects Med 30:374–385 http://dx.doi.org/10.1016/j.mam.2009.07.001. [PubMed]
86. Liu S, Moayeri M, Leppla SH. 2014. Anthrax lethal and edema toxins in anthrax pathogenesis. Trends Microbiol 22:317–325 http://dx.doi.org/10.1016/j.tim.2014.02.012. [PubMed]
87. Meselson M, Guillemin J, Hugh-Jones M, Langmuir A, Popova I, Shelokov A, Yampolskaya O. 1994. The Sverdlovsk anthrax outbreak of 1979. Science 266:1202–1208 http://dx.doi.org/10.1126/science.7973702. [PubMed]
88. Agrawal A, Lingappa J, Leppla SH, Agrawal S, Jabbar A, Quinn C, Pulendran B. 2003. Impairment of dendritic cells and adaptive immunity by anthrax lethal toxin. Nature 424:329–334 http://dx.doi.org/10.1038/nature01794. [PubMed]
89. Moayeri M, Leppla SH, Vrentas C, Pomerantsev AP, Liu S. 2015. Anthrax pathogenesis. Annu Rev Microbiol 69:185–208 http://dx.doi.org/10.1146/annurev-micro-091014-104523. [PubMed]
90. Makino S, Watarai M, Cheun HI, Shirahata T, Uchida I. 2002. Effect of the lower molecular capsule released from the cell surface of Bacillus anthracis on the pathogenesis of anthrax. J Infect Dis 186:227–233 http://dx.doi.org/10.1086/341299. [PubMed]
91. Kozel TR, Murphy WJ, Brandt S, Blazar BR, Lovchik JA, Thorkildson P, Percival A, Lyons CR. 2004. mAbs to Bacillus anthracis capsular antigen for immunoprotection in anthrax and detection of antigenemia. Proc Natl Acad Sci U S A 101:5042–5047 http://dx.doi.org/10.1073/pnas.0401351101. [PubMed]
92. Sutherland MD, Kozel TR. 2009. Macrophage uptake, intracellular localization, and degradation of poly-gamma- d-glutamic acid, the capsular antigen of Bacillus anthracis. Infect Immun 77:532–538 http://dx.doi.org/10.1128/IAI.01009-08. [PubMed]
93. Ezzell JW, Abshire TG, Panchal R, Chabot D, Bavari S, Leffel EK, Purcell B, Friedlander AM, Ribot WJ. 2009. Association of Bacillus anthracis capsule with lethal toxin during experimental infection. Infect Immun 77:749–755 http://dx.doi.org/10.1128/IAI.00764-08. [PubMed]
94. Jang J, Cho M, Chun JH, Cho MH, Park J, Oh HB, Yoo CK, Rhie GE. 2011. The poly-γ- d-glutamic acid capsule of Bacillus anthracis enhances lethal toxin activity. Infect Immun 79:3846–3854 http://dx.doi.org/10.1128/IAI.01145-10. [PubMed]
95. Lee HR, Jeon JH, Park OK, Chun JH, Park J, Rhie GE. 2015. The poly-γ- d-glutamic acid capsule surrogate of the Bacillus anthracis capsule induces nitric oxide production via the platelet activating factor receptor signaling pathway. Mol Immunol 68(2 Pt A) :244–252 http://dx.doi.org/10.1016/j.molimm.2015.08.015. [PubMed]
96. Lee HR, Jeon JH, Rhie GE. 2017. The poly-γ- D-glutamic acid capsule of Bacillus licheniformis: a surrogate of Bacillus anthracis capsule induces interferon-gamma production in NK cells through interactions with macrophages. J Microbiol Biotechnol 27:1032–1037 http://dx.doi.org/10.4014/jmb.1612.12043. [PubMed]
97. Cho MH, Ahn HJ, Ha HJ, Park J, Chun JH, Kim BS, Oh HB, Rhie GE. 2010. Bacillus anthracis capsule activates caspase-1 and induces interleukin-1beta release from differentiated THP-1 and human monocyte-derived dendritic cells. Infect Immun 78:387–392 http://dx.doi.org/10.1128/IAI.00956-09. [PubMed]
98. Chitlaru T, Gat O, Gozlan Y, Ariel N, Shafferman A. 2006. Differential proteomic analysis of the Bacillus anthracis secretome: distinct plasmid and chromosome CO2-dependent cross talk mechanisms modulate extracellular proteolytic activities. J Bacteriol 188:3551–3571 http://dx.doi.org/10.1128/JB.188.10.3551-3571.2006. [PubMed]
99. Chitlaru T, Gat O, Grosfeld H, Inbar I, Gozlan Y, Shafferman A. 2007. Identification of in vivo-expressed immunogenic proteins by serological proteome analysis of the Bacillus anthracis secretome. Infect Immun 75:2841–2852 http://dx.doi.org/10.1128/IAI.02029-06. [PubMed]
100. Thwaite JE, Hibbs S, Titball RW, Atkins TP. 2006. Proteolytic degradation of human antimicrobial peptide LL-37 by Bacillus anthracis may contribute to virulence. Antimicrob Agents Chemother 50:2316–2322 http://dx.doi.org/10.1128/AAC.01488-05. [PubMed]
101. Chung MC, Popova TG, Millis BA, Mukherjee DV, Zhou W, Liotta LA, Petricoin EF, Chandhoke V, Bailey C, Popov SG. 2006. Secreted neutral metalloproteases of Bacillus anthracis as candidate pathogenic factors. J Biol Chem 281:31408–31418 http://dx.doi.org/10.1074/jbc.M605526200. [PubMed]
102. Chung MC, Popova TG, Jorgensen SC, Dong L, Chandhoke V, Bailey CL, Popov SG. 2008. Degradation of circulating von Willebrand factor and its regulator ADAMTS13 implicates secreted Bacillus anthracis metalloproteases in anthrax consumptive coagulopathy. J Biol Chem 283:9531–9542 http://dx.doi.org/10.1074/jbc.M705871200. [PubMed]
103. Mukherjee DV, Tonry JH, Kim KS, Ramarao N, Popova TG, Bailey C, Popov S, Chung MC. 2011. Bacillus anthracis protease InhA increases blood-brain barrier permeability and contributes to cerebral hemorrhages. PLoS One 6:e17921 http://dx.doi.org/10.1371/journal.pone.0017921. [PubMed]
104. Grinberg LM, Abramova FA, Yampolskaya OV, Walker DH, Smith JH. 2001. Quantitative pathology of inhalational anthrax I: quantitative microscopic findings. Mod Pathol 14:482–495 http://dx.doi.org/10.1038/modpathol.3880337. [PubMed]
105. Ehling-Schulz M, Fricker M, Scherer S. 2004. Bacillus cereus, the causative agent of an emetic type of food-borne illness. Mol Nutr Food Res 48:479–487 http://dx.doi.org/10.1002/mnfr.200400055. [PubMed]
106. Schoeni JL, Wong AC. 2005. Bacillus cereus food poisoning and its toxins. J Food Prot 68:636–648 http://dx.doi.org/10.4315/0362-028X-68.3.636. [PubMed]
107. Prüss BM, Dietrich R, Nibler B, Märtlbauer E, Scherer S. 1999. The hemolytic enterotoxin HBL is broadly distributed among species of the Bacillus cereus group. Appl Environ Microbiol 65:5436–5442.
108. Ehling-Schulz M, Messelhäusser U. 2012. One pathogen but two different types of food borne outbreaks; Bacillus cereus in catering facilities in Germany , p 63–70. In Hoorfar J (ed), Case Studies in Food Safety and Quality Management: Lessons from Real-Life Situations. Woodhead Publishing, Cambridge, United Kingdom.
109. Lotte R, Hérissé AL, Berrouane Y, Lotte L, Casagrande F, Landraud L, Herbin S, Ramarao N, Boyer L, Ruimy R. 2017. Virulence analysis of Bacillus cereus isolated after death of preterm neonates, Nice, France, 2013. Emerg Infect Dis 23:845–848 http://dx.doi.org/10.3201/eid2305.161788. [PubMed]
110. Dierick K, Van Coillie E, Swiecicka I, Meyfroidt G, Devlieger H, Meulemans A, Hoedemaekers G, Fourie L, Heyndrickx M, Mahillon J. 2005. Fatal family outbreak of Bacillus cereus-associated food poisoning. J Clin Microbiol 43:4277–4279 http://dx.doi.org/10.1128/JCM.43.8.4277-4279.2005. [PubMed]
111. Pósfay-Barbe KM, Schrenzel J, Frey J, Studer R, Korff C, Belli DC, Parvex P, Rimensberger PC, Schäppi MG. 2008. Food poisoning as a cause of acute liver failure. Pediatr Infect Dis J 27:846–847 http://dx.doi.org/10.1097/INF.0b013e318170f2ae. [PubMed]
112. Tschiedel E, Rath PM, Steinmann J, Becker H, Dietrich R, Paul A, Felderhoff-Müser U, Dohna-Schwake C. 2015. Lifesaving liver transplantation for multi-organ failure caused by Bacillus cereus food poisoning. Pediatr Transplant 19:E11–E14 http://dx.doi.org/10.1111/petr.12378. [PubMed]
113. Stark T, Marxen S, Rütschle A, Lücking G, Scherer S, Ehling-Schulz M, Hofmann T. 2013. Mass spectrometric profiling of Bacillus cereus strains and quantitation of the emetic toxin cereulide by means of stable isotope dilution analysis and HEp-2 bioassay. Anal Bioanal Chem 405:191–201 http://dx.doi.org/10.1007/s00216-012-6485-6. [PubMed]
114. Jeßberger N, Krey VM, Rademacher C, Böhm ME, Mohr AK, Ehling-Schulz M, Scherer S, Märtlbauer E. 2015. From genome to toxicity: a combinatory approach highlights the complexity of enterotoxin production in Bacillus cereus. Front Microbiol 6:560. [PubMed]
115. Kranzler M, Stollewerk K, Rouzeau-Szynalski K, Blayo L, Sulyok M, Ehling-Schulz M. 2016. Temperature exerts control of Bacillus cereus emetic toxin production on post-transcriptional levels. Front Microbiol 7:1640 http://dx.doi.org/10.3389/fmicb.2016.01640. [PubMed]
116. Jeßberger N, Rademacher C, Krey VM, Dietrich R, Mohr AK, Böhm ME, Scherer S, Ehling-Schulz M, Märtlbauer E. 2017. Simulating intestinal growth conditions enhances toxin production of enteropathogenic Bacillus cereus. Front Microbiol 8:627 http://dx.doi.org/10.3389/fmicb.2017.00627. [PubMed]
117. Pinna A, Sechi LA, Zanetti S, Usai D, Delogu G, Cappuccinelli P, Carta F. 2001. Bacillus cereus keratitis associated with contact lens wear. Ophthalmology 108:1830–1834 http://dx.doi.org/10.1016/S0161-6420(01)00723-0.
118. Jones TO, Turnbull PC. 1981. Bovine mastitis caused by Bacillus cereus. Vet Rec 108:271–274 http://dx.doi.org/10.1136/vr.108.13.271. [PubMed]
119. Mavangira V, Angelos JA, Samitz EM, Rowe JD, Byrne BA. 2013. Gangrenous mastitis caused by Bacillus species in six goats. J Am Vet Med Assoc 242:836–843 http://dx.doi.org/10.2460/javma.242.6.836. [PubMed]
120. Chaufaux J, Marchal M, Gilois N, Jehanno I, Buisson C. 1997. Investigation of natural strains of Bacillus thuringiensis in different biotopes through the world. Can J Microbiol 43:337–343 http://dx.doi.org/10.1139/m97-047.
121. Ruan L, Crickmore N, Peng D, Sun M. 2015. Are nematodes a missing link in the confounded ecology of the entomopathogen Bacillus thuringiensis? Trends Microbiol 23:341–346 http://dx.doi.org/10.1016/j.tim.2015.02.011. [PubMed]
122. Borgonie G, Van Driessche R, Leyns F, Arnaut G, De Waele D, Coomans A. 1995. Germination of Bacillus thuringiensis spores in bacteriophagous nematodes (Nematoda: rhabditida). J Invertebr Pathol 65:61–67 http://dx.doi.org/10.1006/jipa.1995.1008. [PubMed]
123. van Frankenhuyzen K. 2009. Insecticidal activity of Bacillus thuringiensis crystal proteins. J Invertebr Pathol 101:1–16 http://dx.doi.org/10.1016/j.jip.2009.02.009. [PubMed]
124. Loguercio LL, Argôlo-Filho RC. 2015. Anthropogenic action shapes the evolutionary ecology of Bacillus thuringiensis: response to Ruan et al. Trends Microbiol 23:519–520 http://dx.doi.org/10.1016/j.tim.2015.06.002. [PubMed]
125. Hendriksen NB. 2016. The two lives of Bacillus thuringiensis: response to Ruan et al. and Loguercio and Argôlo-Filho. Trends Microbiol 24:1–2 http://dx.doi.org/10.1016/j.tim.2015.10.010. [PubMed]
126. Lereclus D, Agaisse H, Grandvalet C, Salamitou S, Gominet M. 2000. Regulation of toxin and virulence gene transcription in Bacillus thuringiensis. Int J Med Microbiol 290:295–299 http://dx.doi.org/10.1016/S1438-4221(00)80024-7.
127. Raymond B, West SA, Griffin AS, Bonsall MB. 2012. The dynamics of cooperative bacterial virulence in the field. Science 337:85–88 http://dx.doi.org/10.1126/science.1218196. [PubMed]
128. Dubois T, Faegri K, Gélis-Jeanvoine S, Perchat S, Lemy C, Buisson C, Nielsen-LeRoux C, Gohar M, Jacques P, Ramarao N, Slamti L, Kolstø AB, Lereclus D. 2016. Correction: necrotrophism is a quorum-sensing-regulated lifestyle in Bacillus thuringiensis. PLoS Pathog 12:e1006049 http://dx.doi.org/10.1371/journal.ppat.1006049. [PubMed]
129. Perchat S, Dubois T, Zouhir S, Gominet M, Poncet S, Lemy C, Aumont-Nicaise M, Deutscher J, Gohar M, Nessler S, Lereclus D. 2011. A cell-cell communication system regulates protease production during sporulation in bacteria of the Bacillus cereus group. Mol Microbiol 82:619–633 http://dx.doi.org/10.1111/j.1365-2958.2011.07839.x. [PubMed]
130. Vilain S, Luo Y, Hildreth MB, Brözel VS. 2006. Analysis of the life cycle of the soil saprophyte Bacillus cereus in liquid soil extract and in soil. Appl Environ Microbiol 72:4970–4977 http://dx.doi.org/10.1128/AEM.03076-05. [PubMed]
131. Ruthel G, Ribot WJ, Bavari S, Hoover TA. 2004. Time-lapse confocal imaging of development of Bacillus anthracis in macrophages. J Infect Dis 189:1313–1316 http://dx.doi.org/10.1086/382656. [PubMed]
132. Oh SY, Lunderberg JM, Chateau A, Schneewind O, Missiakas D. 2016. Genes required for Bacillus anthracis secondary cell wall polysaccharide synthesis. J Bacteriol 199:e00613-16. [PubMed]
133. Chateau A, Lunderberg JM, Oh SY, Abshire T, Friedlander A, Quinn CP, Missiakas DM, Schneewind O. 2018. Galactosylation of the secondary cell wall polysaccharide of Bacillus anthracis and its contribution to anthrax pathogenesis. J Bacteriol 200:e00562-17. [PubMed]
134. Forsberg LS, Choudhury B, Leoff C, Marston CK, Hoffmaster AR, Saile E, Quinn CP, Kannenberg EL, Carlson RW. 2011. Secondary cell wall polysaccharides from Bacillus cereus strains G9241, 03BB87 and 03BB102 causing fatal pneumonia share similar glycosyl structures with the polysaccharides from Bacillus anthracis. Glycobiology 21:934–948 http://dx.doi.org/10.1093/glycob/cwr026. [PubMed]
135. Sychantha D, Chapman RN, Bamford NC, Boons GJ, Howell PL, Clarke AJ. 2018. Molecular basis for the attachment of S-layer proteins to the cell wall of Bacillus anthracis. Biochemistry 57:1949–1953 http://dx.doi.org/10.1021/acs.biochem.8b00060. [PubMed]
136. Missiakas D, Schneewind O. 2017. Assembly and function of the Bacillus anthracis S-layer. Annu Rev Microbiol 71:79–98 http://dx.doi.org/10.1146/annurev-micro-090816-093512. [PubMed]
137. Anderson VJ, Kern JW, McCool JW, Schneewind O, Missiakas D. 2011. The SLH-domain protein BslO is a determinant of Bacillus anthracis chain length. Mol Microbiol 81:192–205 http://dx.doi.org/10.1111/j.1365-2958.2011.07688.x. [PubMed]
138. Goodman JW, Nitecki DE. 1967. Studies on the relation of a prior immune response to immunogenicity. Immunology 13:577–583.
139. Scorpio A, Chabot DJ, Day WA, O’Brien DK, Vietri NJ, Itoh Y, Mohamadzadeh M, Friedlander AM. 2007. Poly-gamma-glutamate capsule-degrading enzyme treatment enhances phagocytosis and killing of encapsulated Bacillus anthracis. Antimicrob Agents Chemother 51:215–222 http://dx.doi.org/10.1128/AAC.00706-06. [PubMed]
140. AuCoin DP, Sutherland MD, Percival AL, Lyons CR, Lovchik JA, Kozel TR. 2009. Rapid detection of the poly-gamma- d-glutamic acid capsular antigen of Bacillus anthracis by latex agglutination. Diagn Microbiol Infect Dis 64:229–232 http://dx.doi.org/10.1016/j.diagmicrobio.2009.02.001. [PubMed]
141. Boyer AE, Quinn CP, Hoffmaster AR, Kozel TR, Saile E, Marston CK, Percival A, Plikaytis BD, Woolfitt AR, Gallegos M, Sabourin P, McWilliams LG, Pirkle JL, Barr JR. 2009. Kinetics of lethal factor and poly- d-glutamic acid antigenemia during inhalation anthrax in rhesus macaques. Infect Immun 77:3432–3441 http://dx.doi.org/10.1128/IAI.00346-09. [PubMed]
142. Jelacic TM, Chabot DJ, Bozue JA, Tobery SA, West MW, Moody K, Yang D, Oppenheim JJ, Friedlander AM. 2014. Exposure to Bacillus anthracis capsule results in suppression of human monocyte-derived dendritic cells. Infect Immun 82:3405–3416 http://dx.doi.org/10.1128/IAI.01857-14. [PubMed]
143. Swick MC, Koehler TM, Driks A. 2016. Surviving between hosts: sporulation and transmission. Microbiol Spectr 4:10.1128/microbiolspec.VMBF-0029-2015.
144. Moir A. 2006. How do spores germinate? J Appl Microbiol 101:526–530 http://dx.doi.org/10.1111/j.1365-2672.2006.02885.x. [PubMed]
145. Bozue JA, Welkos S, Cote CK. 2015. The Bacillus anthracis exosporium: what’s the big “hairy” deal? Microbiol Spectr 3:3 http://dx.doi.org/10.1128/microbiolspec.TBS-0021-2015.
146. Terry C, Jiang S, Radford DS, Wan Q, Tzokov S, Moir A, Bullough PA. 2017. Molecular tiling on the surface of a bacterial spore: the exosporium of the Bacillus anthracis/ cereus/ thuringiensis group. Mol Microbiol 104:539–552 http://dx.doi.org/10.1111/mmi.13650. [PubMed]
147. Weaver J, Kang TJ, Raines KW, Cao GL, Hibbs S, Tsai P, Baillie L, Rosen GM, Cross AS. 2007. Protective role of Bacillus anthracis exosporium in macrophage-mediated killing by nitric oxide. Infect Immun 75:3894–3901 http://dx.doi.org/10.1128/IAI.00283-07. [PubMed]
148. Johnson MJ, Todd SJ, Ball DA, Shepherd AM, Sylvestre P, Moir A. 2006. ExsY and CotY are required for the correct assembly of the exosporium and spore coat of Bacillus cereus. J Bacteriol 188:7905–7913 http://dx.doi.org/10.1128/JB.00997-06. [PubMed]
149. Ball DA, Taylor R, Todd SJ, Redmond C, Couture-Tosi E, Sylvestre P, Moir A, Bullough PA. 2008. Structure of the exosporium and sublayers of spores of the Bacillus cereus family revealed by electron crystallography. Mol Microbiol 68:947–958 http://dx.doi.org/10.1111/j.1365-2958.2008.06206.x. [PubMed]
150. Giorno R, Mallozzi M, Bozue J, Moody KS, Slack A, Qiu D, Wang R, Friedlander A, Welkos S, Driks A. 2009. Localization and assembly of proteins comprising the outer structures of the Bacillus anthracis spore. Microbiology 155:1133–1145 http://dx.doi.org/10.1099/mic.0.023333-0. [PubMed]
151. Giorno R, Bozue J, Cote C, Wenzel T, Moody KS, Mallozzi M, Ryan M, Wang R, Zielke R, Maddock JR, Friedlander A, Welkos S, Driks A. 2007. Morphogenesis of the Bacillus anthracis spore. J Bacteriol 189:691–705 http://dx.doi.org/10.1128/JB.00921-06. [PubMed]
152. Brahmbhatt TN, Janes BK, Stibitz ES, Darnell SC, Sanz P, Rasmussen SB, O’Brien AD. 2007. Bacillus anthracis exosporium protein BclA affects spore germination, interaction with extracellular matrix proteins, and hydrophobicity. Infect Immun 75:5233–5239 http://dx.doi.org/10.1128/IAI.00660-07. [PubMed]
153. Oliva C, Turnbough CL Jr, Kearney JF. 2009. CD14-Mac-1 interactions in Bacillus anthracis spore internalization by macrophages. Proc Natl Acad Sci U S A 106:13957–13962 http://dx.doi.org/10.1073/pnas.0902392106. [PubMed]
154. Oliva CR, Swiecki MK, Griguer CE, Lisanby MW, Bullard DC, Turnbough CL Jr, Kearney JF. 2008. The integrin Mac-1 (CR3) mediates internalization and directs Bacillus anthracis spores into professional phagocytes. Proc Natl Acad Sci U S A 105:1261–1266 http://dx.doi.org/10.1073/pnas.0709321105. [PubMed]
155. Fisher N, Hanna P. 2005. Characterization of Bacillus anthracis germinant receptors in vitro. J Bacteriol 187:8055–8062 http://dx.doi.org/10.1128/JB.187.23.8055-8062.2005. [PubMed]
156. Ireland JA, Hanna PC. 2002. Amino acid- and purine ribonucleoside-induced germination of Bacillus anthracis DeltaSterne endospores: gerS mediates responses to aromatic ring structures. J Bacteriol 184:1296–1303 http://dx.doi.org/10.1128/JB.184.5.1296-1303.2002. [PubMed]
157. Weiner MA, Read TD, Hanna PC. 2003. Identification and characterization of the gerH operon of Bacillus anthracis endospores: a differential role for purine nucleosides in germination. J Bacteriol 185:1462–1464 http://dx.doi.org/10.1128/JB.185.4.1462-1464.2003. [PubMed]
158. Guidi-Rontani C, Pereira Y, Ruffie S, Sirard JC, Weber-Levy M, Mock M. 1999. Identification and characterization of a germination operon on the virulence plasmid pXO1 of Bacillus anthracis. Mol Microbiol 33:407–414 http://dx.doi.org/10.1046/j.1365-2958.1999.01485.x. [PubMed]
159. McKevitt MT, Bryant KM, Shakir SM, Larabee JL, Blanke SR, Lovchik J, Lyons CR, Ballard JD. 2007. Effects of endogenous d-alanine synthesis and autoinhibition of Bacillus anthracis germination on in vitro and in vivo infections. Infect Immun 75:5726–5734 http://dx.doi.org/10.1128/IAI.00727-07. [PubMed]
160. Setlow P. 2014. Spore resistance properties. Microbiol Spectr 2:10.1128/microbiolspec.TBS-0003-2012 http://dx.doi.org/10.1128/microbiolspec.TBS-0003-2012. [PubMed]
161. Giebel JD, Carr KA, Anderson EC, Hanna PC. 2009. The germination-specific lytic enzymes SleB, CwlJ1, and CwlJ2 each contribute to Bacillus anthracis spore germination and virulence. J Bacteriol 191:5569–5576 http://dx.doi.org/10.1128/JB.00408-09. [PubMed]
162. Ross JM. 1955. On the histopathology of experimental anthrax in the guinea-pig. Br J Exp Pathol 36:336–339.
163. Cleret A, Quesnel-Hellmann A, Vallon-Eberhard A, Verrier B, Jung S, Vidal D, Mathieu J, Tournier JN. 2007. Lung dendritic cells rapidly mediate anthrax spore entry through the pulmonary route. J Immunol 178:7994–8001 http://dx.doi.org/10.4049/jimmunol.178.12.7994. [PubMed]
164. Sanz P, Teel LD, Alem F, Carvalho HM, Darnell SC, O’Brien AD. 2008. Detection of Bacillus anthracis spore germination in vivo by bioluminescence imaging. Infect Immun 76:1036–1047 http://dx.doi.org/10.1128/IAI.00985-07. [PubMed]
165. Cote CK, Van Rooijen N, Welkos SL. 2006. Roles of macrophages and neutrophils in the early host response to Bacillus anthracis spores in a mouse model of infection. Infect Immun 74:469–480 http://dx.doi.org/10.1128/IAI.74.1.469-480.2006. [PubMed]
166. Wilson GR, Benoit TG. 1990. Activation and germination of Bacillus thuringiensis spores in Manduca sexta larval gut fluid. J Invertebr Pathol 56:233–236 http://dx.doi.org/10.1016/0022-2011(90)90105-F.
167. Wilson GR, Benoit TG. 1993. Alkaline pH activates Bacillus thuringiensis spores. J Invertebr Pathol 62:87–89 http://dx.doi.org/10.1006/jipa.1993.1079.
168. Abdoarrahem MM, Gammon K, Dancer BN, Berry C. 2009. Genetic basis for alkaline activation of germination in Bacillus thuringiensis subsp. israelensis. Appl Environ Microbiol 75:6410–6413 http://dx.doi.org/10.1128/AEM.00962-09. [PubMed]
169. Du C, Nickerson KW. 1996. Bacillus thuringiensis HD-73 spores have surface-localized Cry1Ac toxin: physiological and pathogenic consequences. Appl Environ Microbiol 62:3722–3726.
170. Bongiorni C, Stoessel R, Shoemaker D, Perego M. 2006. Rap phosphatase of virulence plasmid pXO1 inhibits Bacillus anthracis sporulation. J Bacteriol 188:487–498 http://dx.doi.org/10.1128/JB.188.2.487-498.2006. [PubMed]
171. Brunsing RL, La Clair C, Tang S, Chiang C, Hancock LE, Perego M, Hoch JA. 2005. Characterization of sporulation histidine kinases of Bacillus anthracis. J Bacteriol 187:6972–6981 http://dx.doi.org/10.1128/JB.187.20.6972-6981.2005. [PubMed]
172. White AK, Hoch JA, Grynberg M, Godzik A, Perego M. 2006. Sensor domains encoded in Bacillus anthracis virulence plasmids prevent sporulation by hijacking a sporulation sensor histidine kinase. J Bacteriol 188:6354–6360 http://dx.doi.org/10.1128/JB.00656-06. [PubMed]
173. Perchat S, Talagas A, Zouhir S, Poncet S, Bouillaut L, Nessler S, Lereclus D. 2016. NprR, a moonlighting quorum sensor shifting from a phosphatase activity to a transcriptional activator. Microb Cell 3:573–575 http://dx.doi.org/10.15698/mic2016.11.542. [PubMed]
174. Verplaetse E, Slamti L, Gohar M, Lereclus D. 2015. Cell differentiation in a Bacillus thuringiensis population during planktonic growth, biofilm formation, and host infection. MBio 6:e00138-15 http://dx.doi.org/10.1128/mBio.00138-15. [PubMed]
175. Perego M. 2013. Forty years in the making: understanding the molecular mechanism of peptide regulation in bacterial development. PLoS Biol 11:e1001516 http://dx.doi.org/10.1371/journal.pbio.1001516. [PubMed]
176. Fazion F, Perchat S, Buisson C, Vilas-Boas G, Lereclus D. 2017. A plasmid-borne Rap-Phr system regulates sporulation of Bacillus thuringiensis in insect larvae. Environ Microbiol 20:145–155. [PubMed]
177. Roux E, Yersin A. 1888. Contribution a à l’étude de la diphthérie. Ann Inst Pasteur 2:629–661.
178. Böhm ME, Krey VM, Jeßberger N, Frenzel E, Scherer S. 2016. Comparative bioinformatics and experimental analysis of the intergenic regulatory regions of Bacillus cereushbl and nhe enterotoxin operons and the impact of CodY on virulence heterogeneity. Front Microbiol 7:768 http://dx.doi.org/10.3389/fmicb.2016.00768. [PubMed]
179. Bradley KA, Mogridge J, Mourez M, Collier RJ, Young JA. 2001. Identification of the cellular receptor for anthrax toxin. Nature 414:225–229 http://dx.doi.org/10.1038/n35101999. [PubMed]
180. Scobie HM, Rainey GJ, Bradley KA, Young JA. 2003. Human capillary morphogenesis protein 2 functions as an anthrax toxin receptor. Proc Natl Acad Sci U S A 100:5170–5174 http://dx.doi.org/10.1073/pnas.0431098100. [PubMed]
181. Feld GK, Brown MJ, Krantz BA. 2012. Ratcheting up protein translocation with anthrax toxin. Protein Sci 21:606–624 http://dx.doi.org/10.1002/pro.2052. [PubMed]
182. Park JM, Greten FR, Li ZW, Karin M. 2002. Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition. Science 297:2048–2051 http://dx.doi.org/10.1126/science.1073163. [PubMed]
183. Greaney AJ, Leppla SH, Moayeri M. 2015. Bacterial exotoxins and the inflammasome. Front Immunol 6:570 http://dx.doi.org/10.3389/fimmu.2015.00570. [PubMed]
184. Nakajima K, Tanaka Y. 2010. Exclusion of Kif1c as a candidate gene for anthrax toxin susceptibility. Microb Pathog 48:188–190 http://dx.doi.org/10.1016/j.micpath.2010.02.001. [PubMed]
185. Leppla SH. 1982. Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc Natl Acad Sci U S A 79:3162–3166 http://dx.doi.org/10.1073/pnas.79.10.3162. [PubMed]
186. O’Brien J, Friedlander A, Dreier T, Ezzell J, Leppla S. 1985. Effects of anthrax toxin components on human neutrophils. Infect Immun 47:306–310.
187. Tournier JN, Rossi Paccani S, Quesnel-Hellmann A, Baldari CT. 2009. Anthrax toxins: a weapon to systematically dismantle the host immune defenses. Mol Aspects Med 30:456–466 http://dx.doi.org/10.1016/j.mam.2009.06.002. [PubMed]
188. Moayeri M, Crown D, Dorward DW, Gardner D, Ward JM, Li Y, Cui X, Eichacker P, Leppla SH. 2009. The heart is an early target of anthrax lethal toxin in mice: a protective role for neuronal nitric oxide synthase (nNOS). PLoS Pathog 5:e1000456 http://dx.doi.org/10.1371/journal.ppat.1000456. [PubMed]
189. Tweten RK. 2005. Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect Immun 73:6199–6209 http://dx.doi.org/10.1128/IAI.73.10.6199-6209.2005. [PubMed]
190. Shannon JG, Ross CL, Koehler TM, Rest RF. 2003. Characterization of anthrolysin O, the Bacillus anthracis cholesterol-dependent cytolysin. Infect Immun 71:3183–3189 http://dx.doi.org/10.1128/IAI.71.6.3183-3189.2003. [PubMed]
191. Mosser EM, Rest RF. 2006. The Bacillus anthracis cholesterol-dependent cytolysin, anthrolysin O, kills human neutrophils, monocytes and macrophages. BMC Microbiol 6:56 http://dx.doi.org/10.1186/1471-2180-6-56.
192. Bourdeau RW, Malito E, Chenal A, Bishop BL, Musch MW, Villereal ML, Chang EB, Mosser EM, Rest RF, Tang WJ. 2009. Cellular functions and X-ray structure of anthrolysin O, a cholesterol-dependent cytolysin secreted by Bacillus anthracis. J Biol Chem 284:14645–14656 http://dx.doi.org/10.1074/jbc.M807631200. [PubMed]
193. Bishop BL, Lodolce JP, Kolodziej LE, Boone DL, Tang WJ. 2010. The role of anthrolysin O in gut epithelial barrier disruption during Bacillus anthracis infection. Biochem Biophys Res Commun 394:254–259 http://dx.doi.org/10.1016/j.bbrc.2010.02.091. [PubMed]
194. Bergman NH, Anderson EC, Swenson EE, Janes BK, Fisher N, Niemeyer MM, Miyoshi AD, Hanna PC. 2007. Transcriptional profiling of Bacillus anthracis during infection of host macrophages. Infect Immun 75:3434–3444 http://dx.doi.org/10.1128/IAI.01345-06. [PubMed]
195. Klichko VI, Miller J, Wu A, Popov SG, Alibek K. 2003. Anaerobic induction of Bacillus anthracis hemolytic activity. Biochem Biophys Res Commun 303:855–862 http://dx.doi.org/10.1016/S0006-291X(03)00440-6.
196. Heffernan BJ, Thomason B, Herring-Palmer A, Hanna P. 2007. Bacillus anthracis anthrolysin O and three phospholipases C are functionally redundant in a murine model of inhalation anthrax. FEMS Microbiol Lett 271:98–105 http://dx.doi.org/10.1111/j.1574-6968.2007.00713.x. [PubMed]
197. Beecher DJ, Schoeni JL, Wong AC. 1995. Enterotoxic activity of hemolysin BL from Bacillus cereus. Infect Immun 63:4423–4428.
198. Lund T, Granum PE. 1996. Characterisation of a non-haemolytic enterotoxin complex from Bacillus cereus isolated after a foodborne outbreak. FEMS Microbiol Lett 141:151–156 http://dx.doi.org/10.1111/j.1574-6968.1996.tb08377.x.
199. Lund T, De Buyser ML, Granum PE. 2000. A new cytotoxin from Bacillus cereus that may cause necrotic enteritis. Mol Microbiol 38:254–261 http://dx.doi.org/10.1046/j.1365-2958.2000.02147.x. [PubMed]
200. Beecher DJ, Wong AC. 2000. Cooperative, synergistic and antagonistic haemolytic interactions between haemolysin BL, phosphatidylcholine phospholipase C and sphingomyelinase from Bacillus cereus. Microbiology 146:3033–3039 http://dx.doi.org/10.1099/00221287-146-12-3033. [PubMed]
201. Callegan MC, Jett BD, Hancock LE, Gilmore MS. 1999. Role of hemolysin BL in the pathogenesis of extraintestinal Bacillus cereus infection assessed in an endophthalmitis model. Infect Immun 67:3357–3366.
202. Guillemet E, Cadot C, Tran SL, Guinebretière MH, Lereclus D, Ramarao N. 2010. The InhA metalloproteases of Bacillus cereus contribute concomitantly to virulence. J Bacteriol 192:286–294 http://dx.doi.org/10.1128/JB.00264-09. [PubMed]
203. Oda M, Hashimoto M, Takahashi M, Ohmae Y, Seike S, Kato R, Fujita A, Tsuge H, Nagahama M, Ochi S, Sasahara T, Hayashi S, Hirai Y,Sakurai J. 2012. Role of sphingomyelinase in infectious diseases caused by Bacillus cereus. PLoS One 7:e38054 http://dx.doi.org/10.1371/journal.pone.0038054. [PubMed]
204. Ramarao N, Sanchis V. 2013. The pore-forming haemolysins of bacillus cereus: a review. Toxins (Basel) 5:1119–1139 http://dx.doi.org/10.3390/toxins5061119. [PubMed]
205. Jeßberger N, Dietrich R, Bock S, Didier A, Märtlbauer E. 2014. Bacillus cereus enterotoxins act as major virulence factors and exhibit distinct cytotoxicity to different human cell lines. Toxicon 77:49–57 http://dx.doi.org/10.1016/j.toxicon.2013.10.028. [PubMed]
206. Agata N, Ohta M, Mori M, Isobe M. 1995. A novel dodecadepsipeptide, cereulide, is an emetic toxin of Bacillus cereus. FEMS Microbiol Lett 129:17–20. [PubMed]
207. Magarvey NA, Ehling-Schulz M, Walsh CT. 2006. Characterization of the cereulide NRPS alpha-hydroxy acid specifying modules: activation of alpha-keto acids and chiral reduction on the assembly line. J Am Chem Soc 128:10698–10699 http://dx.doi.org/10.1021/ja0640187. [PubMed]
208. Marxen S, Stark TD, Rütschle A, Lücking G, Frenzel E, Scherer S, Ehling-Schulz M, Hofmann T. 2015. Depsipeptide intermediates interrogate proposed biosynthesis of cereulide, the emetic toxin of Bacillus cereus. Sci Rep 5:10637 http://dx.doi.org/10.1038/srep10637. [PubMed]
209. Medema MH, Kottmann R, Yilmaz P, Cummings M, Biggins JB, Blin K, de Bruijn I, Chooi YH, Claesen J, Coates RC, Cruz-Morales P, Duddela S, Düsterhus S, Edwards DJ, Fewer DP, Garg N, Geiger C, Gomez-Escribano JP, Greule A, Hadjithomas M, Haines AS, Helfrich EJN, Hillwig ML, Ishida K, Jones AC, Jones CS, Jungmann K, Kegler C, Kim HU, Kötter P, Krug D, Masschelein J, Melnik AV, Mantovani SM, Monroe EA, Moore M, Moss N, Nützmann H-W, Pan G, Pati A, Petras D, Reen FJ, Rosconi F, Rui Z, Tian Z, Tobias NJ, Tsunematsu Y, Wiemann P, Wyckoff E, Yan X, Yim G, Yu F, et al. 2015. Minimum information about a biosynthetic gene cluster. Nat Chem Biol 11:625–631 http://dx.doi.org/10.1038/nchembio.1890. [PubMed]
210. Bauer T, Stark T, Hofmann T, Ehling-Schulz M. 2010. Development of a stable isotope dilution analysis for the quantification of the Bacillus cereus toxin cereulide in foods. J Agric Food Chem 58:1420–1428 http://dx.doi.org/10.1021/jf9033046. [PubMed]
211. Marxen S, Stark TD, Frenzel E, Rütschle A, Lücking G, Pürstinger G, Pohl EE, Scherer S, Ehling-Schulz M, Hofmann T. 2015. Chemodiversity of cereulide, the emetic toxin of Bacillus cereus. Anal Bioanal Chem 407:2439–2453 http://dx.doi.org/10.1007/s00216-015-8511-y. [PubMed]
212. Rajkovic A, Uyttendaele M, Vermeulen A, Andjelkovic M, Fitz-James I, in ’t Veld P, Denon Q, Verhe R, Debevere J. 2008. Heat resistance of Bacillus cereus emetic toxin, cereulide. Lett Appl Microbiol 46:536–541. [PubMed]
213. Vangoitsenhoven R, Rondas D, Crèvecoeur I, D’Hertog W, Baatsen P, Masini M, Andjelkovic M, Van Loco J, Matthys C, Mathieu C, Overbergh L, Van der Schueren B. 2014. Foodborne cereulide causes beta-cell dysfunction and apoptosis. PLoS One 9:e104866 http://dx.doi.org/10.1371/journal.pone.0104866. [PubMed]
214. Johler S, Kalbhenn EM, Heini N, Brodmann P, Gautsch S, Bagcioglu M, Contzen M, Stephan R, Ehling-Schulz M. 2018. Enterotoxin production of Bacillus thuringiensis isolates from biopesticides, foods, and outbreaks. Front Microbiol 9:1915 http://dx.doi.org/10.3389/fmicb.2018.01915. [PubMed]
215. Deng C, Peng Q, Song F, Lereclus D. 2014. Regulation of cry gene expression in Bacillus thuringiensis. Toxins (Basel) 6:2194–2209 http://dx.doi.org/10.3390/toxins6072194. [PubMed]
216. Zhu Y, Ji F, Shang H, Zhu Q, Wang P, Xu C, Deng Y, Peng D, Ruan L, Sun M. 2011. Gene clusters located on two large plasmids determine spore crystal association (SCA) in Bacillus thuringiensis subsp. finitimus strain YBT-020. PLoS One 6:e27164 http://dx.doi.org/10.1371/journal.pone.0027164. [PubMed]
217. Deng C, Slamti L, Raymond B, Liu G, Lemy C, Gominet M, Yang J, Wang H, Peng Q, Zhang J, Lereclus D, Song F. 2015. Division of labour and terminal differentiation in a novel Bacillus thuringiensis strain. ISME J 9:286–296 http://dx.doi.org/10.1038/ismej.2014.122. [PubMed]
218. Agaisse H, Lereclus D. 1995. How does Bacillus thuringiensis produce so much insecticidal crystal protein? J Bacteriol 177:6027–6032 http://dx.doi.org/10.1128/jb.177.21.6027-6032.1995. [PubMed]
219. Crickmore N, Zeigler DR, Feitelson J, Schnepf E, Van Rie J, Lereclus D, Baum J, Dean DH. 1998. Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol Mol Biol Rev 62:807–813.
220. Ibrahim MA, Griko N, Junker M, Bulla LA. 2010. Bacillus thuringiensis: a genomics and proteomics perspective. Bioeng Bugs 1:31–50 http://dx.doi.org/10.4161/bbug.1.1.10519. [PubMed]
221. Pérez C, Fernandez LE, Sun J, Folch JL, Gill SS, Soberón M, Bravo A. 2005. Bacillus thuringiensis subsp. israelensis Cyt1Aa synergizes Cry11Aa toxin by functioning as a membrane-bound receptor. Proc Natl Acad Sci U S A 102:18303–18308 http://dx.doi.org/10.1073/pnas.0505494102. [PubMed]
222. Popov SG, Popova TG, Hopkins S, Weinstein RS, MacAfee R, Fryxell KJ, Chandhoke V, Bailey C, Alibek K. 2005. Effective antiprotease-antibiotic treatment of experimental anthrax. BMC Infect Dis 5:25 http://dx.doi.org/10.1186/1471-2334-5-25. [PubMed]
223. Pflughoeft KJ, Sumby P, Koehler TM. 2011. Bacillus anthracis sin locus and regulation of secreted proteases. J Bacteriol 193:631–639 http://dx.doi.org/10.1128/JB.01083-10. [PubMed]
224. Dubois T, Faegri K, Perchat S, Lemy C, Buisson C, Nielsen-LeRoux C, Gohar M, Jacques P, Ramarao N, Kolstø AB, Lereclus D. 2012. Necrotrophism is a quorum-sensing-regulated lifestyle in Bacillus thuringiensis. PLoS Pathog 8:e1002629 http://dx.doi.org/10.1371/journal.ppat.1002629. [PubMed]
225. Pflughoeft KJ, Swick MC, Engler DA, Yeo HJ, Koehler TM. 2014. Modulation of the Bacillus anthracis secretome by the immune inhibitor A1 protease. J Bacteriol 196:424–435 http://dx.doi.org/10.1128/JB.00690-13. [PubMed]
226. Gomis-Rüth FX. 2013. A different look for AB5 toxins. Structure 21:1909–1910 http://dx.doi.org/10.1016/j.str.2013.10.004. [PubMed]
227. Terwilliger A, Swick MC, Pflughoeft KJ, Pomerantsev A, Lyons CR, Koehler TM, Maresso A. 2015. Bacillus anthracis overcomes an amino acid auxotrophy by cleaving host serum proteins. J Bacteriol 197:2400–2411 http://dx.doi.org/10.1128/JB.00073-15. [PubMed]
228. Ramarao N, Lereclus D. 2005. The InhA1 metalloprotease allows spores of the B. cereus group to escape macrophages. Cell Microbiol 7:1357–1364 http://dx.doi.org/10.1111/j.1462-5822.2005.00562.x. [PubMed]
229. Welkos S, Bozue J, Twenhafel N, Cote C. 2015. Animal models for the pathogenesis, treatment, and prevention of infection by Bacillus anthracis. Microbiol Spectr 3:TBS-0001–TBS-2012.
230. Loving CL, Khurana T, Osorio M, Lee GM, Kelly VK, Stibitz S, Merkel TJ. 2009. Role of anthrax toxins in dissemination, disease progression, and induction of protective adaptive immunity in the mouse aerosol challenge model. Infect Immun 77:255–265 http://dx.doi.org/10.1128/IAI.00633-08. [PubMed]
231. Friedlander AM, Welkos SL, Ivins BE. 2002. Anthrax vaccines. Curr Top Microbiol Immunol 271:33–60 http://dx.doi.org/10.1007/978-3-662-05767-4_3. [PubMed]
232. Ivins BE, Welkos SL. 1986. Cloning and expression of the Bacillus anthracis protective antigen gene in Bacillus subtilis. Infect Immun 54:537–542.
233. Fellows PF, Linscott MK, Ivins BE, Pitt ML, Rossi CA, Gibbs PH, Friedlander AM. 2001. Efficacy of a human anthrax vaccine in guinea pigs, rabbits, and rhesus macaques against challenge by Bacillus anthracis isolates of diverse geographical origin. Vaccine 19:3241–3247 http://dx.doi.org/10.1016/S0264-410X(01)00021-4.
234. Carr KA, Lybarger SR, Anderson EC, Janes BK, Hanna PC. 2010. The role of Bacillus anthracis germinant receptors in germination and virulence. Mol Microbiol 75:365–375 http://dx.doi.org/10.1111/j.1365-2958.2009.06972.x. [PubMed]
235. Glomski IJ, Corre JP, Mock M, Goossens PL. 2007. Noncapsulated toxinogenic Bacillus anthracis presents a specific growth and dissemination pattern in naive and protective antigen-immune mice. Infect Immun 75:4754–4761 http://dx.doi.org/10.1128/IAI.00575-07. [PubMed]
236. Glomski IJ, Dumetz F, Jouvion G, Huerre MR, Mock M, Goossens PL. 2008. Inhaled non-capsulated Bacillus anthracis in A/J mice: nasopharynx and alveolar space as dual portals of entry, delayed dissemination, and specific organ targeting. Microbes Infect 10:1398–1404 http://dx.doi.org/10.1016/j.micinf.2008.07.042. [PubMed]
237. Little SF, Webster WM, Ivins BE, Fellows PF, Norris SL, Andrews GP. 2004. Development of an in vitro-based potency assay for anthrax vaccine. Vaccine 22:2843–2852 http://dx.doi.org/10.1016/j.vaccine.2003.12.027. [PubMed]
238. Pittman PR, Gibbs PH, Cannon TL, Friedlander AM. 2001. Anthrax vaccine: short-term safety experience in humans. Vaccine 20:972–978 http://dx.doi.org/10.1016/S0264-410X(01)00387-5.
239. Pittman PR, Norris SL, Barrera Oro JG, Bedwell D, Cannon TL, McKee KT Jr. 2006. Patterns of antibody response in humans to the anthrax vaccine adsorbed (AVA) primary (six-dose) series. Vaccine 24:3654–3660 http://dx.doi.org/10.1016/j.vaccine.2006.01.054. [PubMed]
240. Williamson ED, Hodgson I, Walker NJ, Topping AW, Duchars MG, Mott JM, Estep J, Lebutt C, Flick-Smith HC, Jones HE, Li H, Quinn CP. 2005. Immunogenicity of recombinant protective antigen and efficacy against aerosol challenge with anthrax. Infect Immun 73:5978–5987 http://dx.doi.org/10.1128/IAI.73.9.5978-5987.2005. [PubMed]
241. Nye SH, Wittenburg AL, Evans DL, O’Connor JA, Roman RJ, Jacob HJ. 2008. Rat survival to anthrax lethal toxin is likely controlled by a single gene. Pharmacogenomics J 8:16–22 http://dx.doi.org/10.1038/sj.tpj.6500448. [PubMed]
242. Newman ZL, Crown D, Leppla SH, Moayeri M. 2010. Anthrax lethal toxin activates the inflammasome in sensitive rat macrophages. Biochem Biophys Res Commun 398:785–789 http://dx.doi.org/10.1016/j.bbrc.2010.07.039. [PubMed]
243. Salamitou S, Ramisse F, Brehélin M, Bourguet D, Gilois N, Gominet M, Hernandez E, Lereclus D. 2000. The plcR regulon is involved in the opportunistic properties of Bacillus thuringiensis and Bacillus cereus in mice and insects. Microbiology 146:2825–2832 http://dx.doi.org/10.1099/00221287-146-11-2825. [PubMed]
244. Hernandez E, Ramisse F, Gros P, Cavallo J. 2000. Super-infection by Bacillus thuringiensis H34 or 3a3b can lead to death in mice infected with the influenza A virus. FEMS Immunol Med Microbiol 29:177–181 http://dx.doi.org/10.1111/j.1574-695X.2000.tb01520.x.
245. Callegan MC, Kane ST, Cochran DC, Gilmore MS, Gominet M, Lereclus D. 2003. Relationship of plcR-regulated factors to Bacillus endophthalmitis virulence. Infect Immun 71:3116–3124 http://dx.doi.org/10.1128/IAI.71.6.3116-3124.2003. [PubMed]
246. Wilcks A, Hansen BM, Hendriksen NB, Licht TR. 2006. Fate and effect of ingested Bacillus cereus spores and vegetative cells in the intestinal tract of human-flora-associated rats. FEMS Immunol Med Microbiol 46:70–77. [PubMed]
247. Rolny IS, Minnaard J, Racedo SM, Pérez PF. 2014. Murine model of Bacillus cereus gastrointestinal infection. J Med Microbiol 63:1741–1749. [PubMed]
248. Shinagawa K, Konuma H, Sekita H, Sugii S. 1995. Emesis of rhesus monkeys induced by intragastric administration with the HEp-2 vacuolation factor (cereulide) produced by Bacillus cereus. FEMS Microbiol Lett 130:87–90. [PubMed]
249. Melling J, Capel BJ, Turnbull PC, Gilbert RJ. 1976. Identification of a novel enterotoxigenic activity associated with Bacillus cereus. J Clin Pathol 29:938–940 http://dx.doi.org/10.1136/jcp.29.10.938. [PubMed]
250. Angus TA. 1954. A bacterial toxin paralysing silkworm larvae. Nature 173:545–546 http://dx.doi.org/10.1038/173545a0. [PubMed]
251. Hannay CL. 1953. Crystalline inclusions in aerobic spore-forming bacteria. Nature 172:1004 http://dx.doi.org/10.1038/1721004a0. [PubMed]
252. Bravo A, Likitvivatanavong S, Gill SS, Soberón M. 2011. Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem Mol Biol 41:423–431 http://dx.doi.org/10.1016/j.ibmb.2011.02.006. [PubMed]
253. Rees JS, Jarrett P, Ellar DJ. 2009. Peritrophic membrane contribution to Bt Cry delta-endotoxin susceptibility in Lepidoptera and the effect of calcofluor. J Invertebr Pathol 100:139–146 http://dx.doi.org/10.1016/j.jip.2009.01.002. [PubMed]
254. Caccia S, Di Lelio I, La Storia A, Marinelli A, Varricchio P, Franzetti E, Banyuls N, Tettamanti G, Casartelli M, Giordana B, Ferré J, Gigliotti S, Ercolini D, Pennacchio F. 2016. Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism. Proc Natl Acad Sci U S A 113:9486–9491 http://dx.doi.org/10.1073/pnas.1521741113. [PubMed]
255. Johnson DE, McGaughey WH. 1996. Contribution of Bacillus thuringiensis spores to toxicity of purified Cry proteins towards Indianmeal moth larvae. Curr Microbiol 33:54–59 http://dx.doi.org/10.1007/s002849900074. [PubMed]
256. Dubois NR, Dean DH. 1995. Synergism between Cry1A insecticidal crystal proteins and spores of Bacillus thuringiensis, other bacterial spores and vegetative cells against Lymantria dispar (Lepidoptera: Lymantriidae) larvae. Environ Entomol 24:1741–1747 http://dx.doi.org/10.1093/ee/24.6.1741.
257. Miyasono M, Inagaki S, Yamamoto M, Ohba K, Ishiguro T, Takeda R, Hayashi Y. 1994. Enhancement of δ-endotoxin activity by toxin-free spore of Bacillus thuringiensis against the diamondback moth, Plutella xylostella. J Invertebr Pathol 63:111–112 http://dx.doi.org/10.1006/jipa.1994.1021.
258. Burges HD, Thomson EM, Latchford RA. 1976. Importance of spores and d-endotoxin protein crystals of Bacillus thuringiensis in Galleria mellonella. J Invertebr Pathol 27:87–94 http://dx.doi.org/10.1016/0022-2011(76)90032-X.
259. Li RS, Jarrett P, Burges HD. 1987. Importance of spores, crystals, and δ-endotoxins in the pathogenicity of different varieties of Bacillus thuringiensis in Galleria mellonela and Pieris brassicae. J Invertebr Pathol 50:277–284 http://dx.doi.org/10.1016/0022-2011(87)90093-0.
260. Fedhila S, Buisson C, Dussurget O, Serror P, Glomski IJ, Liehl P, Lereclus D, Nielsen-LeRoux C. 2010. Comparative analysis of the virulence of invertebrate and mammalian pathogenic bacteria in the oral insect infection model Galleria mellonella. J Invertebr Pathol 103:24–29 http://dx.doi.org/10.1016/j.jip.2009.09.005. [PubMed]
261. Nielsen-LeRoux C, Gaudriault S, Ramarao N, Lereclus D, Givaudan A. 2012. How the insect pathogen bacteria Bacillus thuringiensis and Xenorhabdus/Photorhabdus occupy their hosts. Curr Opin Microbiol 15:220–231 http://dx.doi.org/10.1016/j.mib.2012.04.006. [PubMed]
262. Peng D, Lin J, Huang Q, Zheng W, Liu G, Zheng J, Zhu L, Sun M. 2016. A novel metalloproteinase virulence factor is involved in Bacillus thuringiensis pathogenesis in nematodes and insects. Environ Microbiol 18:846–862 http://dx.doi.org/10.1111/1462-2920.13069. [PubMed]
263. Fang S, Wang L, Guo W, Zhang X, Peng D, Luo C, Yu Z, Sun M. 2009. Bacillus thuringiensis bel protein enhances the toxicity of Cry1Ac protein to Helicoverpa armigera larvae by degrading insect intestinal mucin. Appl Environ Microbiol 75:5237–5243 http://dx.doi.org/10.1128/AEM.00532-09. [PubMed]
264. Ruan L, Crickmore N, Sun M. 2015. Is there sufficient evidence to consider Bacillus thuringiensis a multihost pathogen? Response to Loguercio and Argôlo-Filho. Trends Microbiol 23:587 http://dx.doi.org/10.1016/j.tim.2015.08.004. [PubMed]
265. Luo X, Chen L, Huang Q, Zheng J, Zhou W, Peng D, Ruan L, Sun M. 2013. Bacillus thuringiensis metalloproteinase Bmp1 functions as a nematicidal virulence factor. Appl Environ Microbiol 79:460–468 http://dx.doi.org/10.1128/AEM.02551-12. [PubMed]
266. Fedhila S, Daou N, Lereclus D, Nielsen-LeRoux C. 2006. Identification of Bacillus cereus internalin and other candidate virulence genes specifically induced during oral infection in insects. Mol Microbiol 62:339–355 http://dx.doi.org/10.1111/j.1365-2958.2006.05362.x. [PubMed]
267. Daou N, Buisson C, Gohar M, Vidic J, Bierne H, Kallassy M, Lereclus D, Nielsen-LeRoux C. 2009. IlsA, a unique surface protein of Bacillus cereus required for iron acquisition from heme, hemoglobin and ferritin. PLoS Pathog 5:e1000675 http://dx.doi.org/10.1371/journal.ppat.1000675. [PubMed]
268. Harvie DR, Vílchez S, Steggles JR, Ellar DJ. 2005. Bacillus cereus Fur regulates iron metabolism and is required for full virulence. Microbiology 151:569–577 http://dx.doi.org/10.1099/mic.0.27744-0. [PubMed]
269. Kamar R, Réjasse A, Jéhanno I, Attieh Z, Courtin P, Chapot-Chartier MP, Nielsen-Leroux C, Lereclus D, El Chamy L, Kallassy M, Sanchis-Borja V. 2017. DltX of Bacillus thuringiensis is essential for d-alanylation of teichoic acids and resistance to antimicrobial response in insects. Front Microbiol 8:1437 http://dx.doi.org/10.3389/fmicb.2017.01437. [PubMed]
270. Guillemet E, Leréec A, Tran SL, Royer C, Barbosa I, Sansonetti P, Lereclus D, Ramarao N. 2016. The bacterial DNA repair protein Mfd confers resistance to the host nitrogen immune response. Sci Rep 6:29349 http://dx.doi.org/10.1038/srep29349. [PubMed]
271. Tran SL, Guillemet E, Gohar M, Lereclus D, Ramarao N. 2010. CwpFM (EntFM) is a Bacillus cereus potential cell wall peptidase implicated in adhesion, biofilm formation, and virulence. J Bacteriol 192:2638–2642 http://dx.doi.org/10.1128/JB.01315-09. [PubMed]
272. Mazzantini D, Celandroni F, Salvetti S, Gueye SA, Lupetti A, Senesi S, Ghelardi E. 2016. FlhF is required for swarming motility and full pathogenicity of Bacillus cereus. Front Microbiol 7:1644 http://dx.doi.org/10.3389/fmicb.2016.01644. [PubMed]
273. Frenzel E, Doll V, Pauthner M, Lücking G, Scherer S, Ehling-Schulz M. 2012. CodY orchestrates the expression of virulence determinants in emetic Bacillus cereus by impacting key regulatory circuits. Mol Microbiol 85:67–88 http://dx.doi.org/10.1111/j.1365-2958.2012.08090.x. [PubMed]
274. Frenzel E, Kranzler M, Stark TD, Hofmann T, Ehling-Schulz M. 2015. The endospore-forming pathogen Bacillus cereus exploits a small colony variant-based diversification strategy in response to aminoglycoside exposure. MBio 6:e01172-15 http://dx.doi.org/10.1128/mBio.01172-15. [PubMed]
275. Andersson MA, Mikkola R, Helin J, Andersson MC, Salkinoja-Salonen M. 1998. A novel sensitive bioassay for detection of Bacillus cereus emetic toxin and related depsipeptide ionophores. Appl Environ Microbiol 64:1338–1343.
276. Wijnands LM, Dufrenne JB, Zwietering MH, van Leusden FM. 2006. Spores from mesophilic Bacillus cereus strains germinate better and grow faster in simulated gastro-intestinal conditions than spores from psychrotrophic strains. Int J Food Microbiol 112:120–128 http://dx.doi.org/10.1016/j.ijfoodmicro.2006.06.015. [PubMed]
277. Ceuppens S, Van de Wiele T, Rajkovic A, Ferrer-Cabaceran T, Heyndrickx M, Boon N, Uyttendaele M. 2012. Impact of intestinal microbiota and gastrointestinal conditions on the in vitro survival and growth of Bacillus cereus. Int J Food Microbiol 155:241–246 http://dx.doi.org/10.1016/j.ijfoodmicro.2012.02.013. [PubMed]
278. Tsilia V, Kerckhof FM, Rajkovic A, Heyndrickx M, Van de Wiele T. 2015. Bacillus cereus NVH 0500/00 can adhere to mucin but cannot produce enterotoxins during gastrointestinal simulation. Appl Environ Microbiol 82:289–296 http://dx.doi.org/10.1128/AEM.02940-15. [PubMed]
279. Possemiers S, Marzorati M, Verstraete W, Van de Wiele T. 2010. Bacteria and chocolate: a successful combination for probiotic delivery. Int J Food Microbiol 141:97–103 http://dx.doi.org/10.1016/j.ijfoodmicro.2010.03.008. [PubMed]
280. Sonenshein AL. 2007. Control of key metabolic intersections in Bacillus subtilis. Nat Rev Microbiol 5:917–927 http://dx.doi.org/10.1038/nrmicro1772. [PubMed]
281. Lindbäck T, Mols M, Basset C, Granum PE, Kuipers OP, Kovács AT. 2012. CodY, a pleiotropic regulator, influences multicellular behaviour and efficient production of virulence factors in Bacillus cereus. Environ Microbiol 14:2233–2246 http://dx.doi.org/10.1111/j.1462-2920.2012.02766.x. [PubMed]
282. Bourgogne A, Drysdale M, Hilsenbeck SG, Peterson SN, Koehler TM. 2003. Global effects of virulence gene regulators in a Bacillus anthracis strain with both virulence plasmids. Infect Immun 71:2736–2743 http://dx.doi.org/10.1128/IAI.71.5.2736-2743.2003. [PubMed]
283. Lücking G, Dommel MK, Scherer S, Fouet A, Ehling-Schulz M. 2009. Cereulide synthesis in emetic Bacillus cereus is controlled by the transition state regulator AbrB, but not by the virulence regulator PlcR. Microbiology 155:922–931 http://dx.doi.org/10.1099/mic.0.024125-0. [PubMed]
284. van Schaik W, Château A, Dillies MA, Coppée JY, Sonenshein AL, Fouet A. 2009. The global regulator CodY regulates toxin gene expression in Bacillus anthracis and is required for full virulence. Infect Immun 77:4437–4445 http://dx.doi.org/10.1128/IAI.00716-09. [PubMed]
285. Lücking G, Frenzel E, Rütschle A, Marxen S, Stark TD, Hofmann T, Scherer S, Ehling-Schulz M. 2015. Ces locus embedded proteins control the non-ribosomal synthesis of the cereulide toxin in emetic Bacillus cereus on multiple levels. Front Microbiol 6:1101 http://dx.doi.org/10.3389/fmicb.2015.01101. [PubMed]
286. Shivers RP, Sonenshein AL. 2004. Activation of the Bacillus subtilis global regulator CodY by direct interaction with branched-chain amino acids. Mol Microbiol 53:599–611 http://dx.doi.org/10.1111/j.1365-2958.2004.04135.x. [PubMed]
287. Handke LD, Shivers RP, Sonenshein AL. 2008. Interaction of Bacillus subtilis CodY with GTP. J Bacteriol 190:798–806 http://dx.doi.org/10.1128/JB.01115-07. [PubMed]
288. Molle V, Nakaura Y, Shivers RP, Yamaguchi H, Losick R, Fujita Y, Sonenshein AL. 2003. Additional targets of the Bacillus subtilis global regulator CodY identified by chromatin immunoprecipitation and genome-wide transcript analysis. J Bacteriol 185:1911–1922 http://dx.doi.org/10.1128/JB.185.6.1911-1922.2003. [PubMed]
289. Dineen SS, Villapakkam AC, Nordman JT, Sonenshein AL. 2007. Repression of Clostridium difficile toxin gene expression by CodY. Mol Microbiol 66:206–219 http://dx.doi.org/10.1111/j.1365-2958.2007.05906.x. [PubMed]
290. Shivers RP, Dineen SS, Sonenshein AL. 2006. Positive regulation of Bacillus subtilis ackA by CodY and CcpA: establishing a potential hierarchy in carbon flow. Mol Microbiol 62:811–822 http://dx.doi.org/10.1111/j.1365-2958.2006.05410.x. [PubMed]
291. Strauch MA, Hoch JA. 1993. Transition-state regulators: sentinels of Bacillus subtilis post-exponential gene expression. Mol Microbiol 7:337–342 http://dx.doi.org/10.1111/j.1365-2958.1993.tb01125.x. [PubMed]
292. Bobay BG, Benson L, Naylor S, Feeney B, Clark AC, Goshe MB, Strauch MA, Thompson R, Cavanagh J. 2004. Evaluation of the DNA binding tendencies of the transition state regulator AbrB. Biochemistry 43:16106–16118 http://dx.doi.org/10.1021/bi048399h. [PubMed]
293. Grandvalet C, Gominet M, Lereclus D. 2001. Identification of genes involved in the activation of the Bacillus thuringiensis inhA metalloprotease gene at the onset of sporulation. Microbiology 147:1805–1813 http://dx.doi.org/10.1099/00221287-147-7-1805. [PubMed]
294. Saile E, Koehler TM. 2002. Control of anthrax toxin gene expression by the transition state regulator abrB. J Bacteriol 184:370–380 http://dx.doi.org/10.1128/JB.184.2.370-380.2002. [PubMed]
295. Britton RA, Eichenberger P, Gonzalez-Pastor JE, Fawcett P, Monson R, Losick R, Grossman AD. 2002. Genome-wide analysis of the stationary-phase sigma factor (sigma-H) regulon of Bacillus subtilis. J Bacteriol 184:4881–4890 http://dx.doi.org/10.1128/JB.184.17.4881-4890.2002. [PubMed]
296. Hadjifrangiskou M, Chen Y, Koehler TM. 2007. The alternative sigma factor sigmaH is required for toxin gene expression by Bacillus anthracis. J Bacteriol 189:1874–1883 http://dx.doi.org/10.1128/JB.01333-06. [PubMed]
297. Bongiorni C, Fukushima T, Wilson AC, Chiang C, Mansilla MC, Hoch JA, Perego M. 2008. Dual promoters control expression of the Bacillus anthracis virulence factor AtxA. J Bacteriol 190:6483–6492 http://dx.doi.org/10.1128/JB.00766-08. [PubMed]
298. Fouet A, Namy O, Lambert G. 2000. Characterization of the operon encoding the alternative sigma(B) factor from Bacillus anthracis and its role in virulence. J Bacteriol 182:5036–5045 http://dx.doi.org/10.1128/JB.182.18.5036-5045.2000. [PubMed]
299. Slamti L, Lereclus D. 2002. A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J 21:4550–4559 http://dx.doi.org/10.1093/emboj/cdf450. [PubMed]
300. Pottathil M, Lazazzera BA. 2003. The extracellular Phr peptide-Rap phosphatase signaling circuit of Bacillus subtilis. Front Biosci 8:d32–d45 http://dx.doi.org/10.2741/913.
301. Declerck N, Bouillaut L, Chaix D, Rugani N, Slamti L, Hoh F, Lereclus D, Arold ST. 2007. Structure of PlcR: insights into virulence regulation and evolution of quorum sensing in Gram-positive bacteria. Proc Natl Acad Sci U S A 104:18490–18495 http://dx.doi.org/10.1073/pnas.0704501104. [PubMed]
302. Slamti L, Perchat S, Huillet E, Lereclus D. 2014. Quorum sensing in Bacillus thuringiensis is required for completion of a full infectious cycle in the insect. Toxins (Basel) 6:2239–2255 http://dx.doi.org/10.3390/toxins6082239. [PubMed]
303. Slamti L, Perchat S, Gominet M, Vilas-Bôas G, Fouet A, Mock M, Sanchis V, Chaufaux J, Gohar M, Lereclus D. 2004. Distinct mutations in PlcR explain why some strains of the Bacillus cereus group are nonhemolytic. J Bacteriol 186:3531–3538 http://dx.doi.org/10.1128/JB.186.11.3531-3538.2004. [PubMed]
304. Grenha R, Slamti L, Nicaise M, Refes Y, Lereclus D, Nessler S. 2013. Structural basis for the activation mechanism of the PlcR virulence regulator by the quorum-sensing signal peptide PapR. Proc Natl Acad Sci U S A 110:1047–1052 http://dx.doi.org/10.1073/pnas.1213770110. [PubMed]
305. Bouillaut L, Perchat S, Arold S, Zorrilla S, Slamti L, Henry C, Gohar M, Declerck N, Lereclus D. 2008. Molecular basis for group-specific activation of the virulence regulator PlcR by PapR heptapeptides. Nucleic Acids Res 36:3791–3801 http://dx.doi.org/10.1093/nar/gkn149. [PubMed]
306. Slamti L, Lereclus D. 2005. Specificity and polymorphism of the PlcR-PapR quorum-sensing system in the Bacillus cereus group. J Bacteriol 187:1182–1187 http://dx.doi.org/10.1128/JB.187.3.1182-1187.2005. [PubMed]
307. Zouhir S, Perchat S, Nicaise M, Perez J, Guimaraes B, Lereclus D, Nessler S. 2013. Peptide-binding dependent conformational changes regulate the transcriptional activity of the quorum-sensor NprR. Nucleic Acids Res 41:7920–7933 http://dx.doi.org/10.1093/nar/gkt546. [PubMed]
308. Gélis-Jeanvoine S, Canette A, Gohar M, Caradec T, Lemy C, Gominet M, Jacques P, Lereclus D, Slamti L. 2017. Genetic and functional analyses of krs, a locus encoding kurstakin, a lipopeptide produced by Bacillus thuringiensis. Res Microbiol 168:356–368 http://dx.doi.org/10.1016/j.resmic.2016.06.002. [PubMed]
309. Perchat S, Talagas A, Poncet S, Lazar N, Li de la Sierra-Gallay I, Gohar M, Lereclus D, Nessler S. 2016. How quorum sensing connects sporulation to necrotrophism in Bacillus thuringiensis. PLoS Pathog 12:e1005779 http://dx.doi.org/10.1371/journal.ppat.1005779. [PubMed]
310. Uchida I, Hornung JM, Thorne CB, Klimpel KR, Leppla SH. 1993. Cloning and characterization of a gene whose product is a trans-activator of anthrax toxin synthesis. J Bacteriol 175:5329–5338 http://dx.doi.org/10.1128/jb.175.17.5329-5338.1993. [PubMed]
311. Koehler TM, Dai Z, Kaufman-Yarbray M. 1994. Regulation of the Bacillus anthracis protective antigen gene: CO 2 and a trans-acting element activate transcription from one of two promoters. J Bacteriol 176:586–595 http://dx.doi.org/10.1128/jb.176.3.586-595.1994. [PubMed]
312. Sirard JC, Guidi-Rontani C, Fouet A, Mock M. 2000. Characterization of a plasmid region involved in Bacillus anthracis toxin production and pathogenesis. Int J Med Microbiol 290:313–316 http://dx.doi.org/10.1016/S1438-4221(00)80030-2.
313. 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.
314. Mignot T, Mock M, Fouet A. 2003. A plasmid-encoded regulator couples the synthesis of toxins and surface structures in Bacillus anthracis. Mol Microbiol 47:917–927 http://dx.doi.org/10.1046/j.1365-2958.2003.03345.x. [PubMed]
315. Makino S, 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 http://dx.doi.org/10.1128/jb.171.2.722-730.1989. [PubMed]
316. Guignot J, Mock M, Fouet A. 1997. AtxA activates the transcription of genes harbored by both Bacillus anthracis virulence plasmids. FEMS Microbiol Lett 147:203–207 http://dx.doi.org/10.1111/j.1574-6968.1997.tb10242.x.
317. Candela T, Mock M, Fouet A. 2005. CapE, a 47-amino-acid peptide, is necessary for Bacillus anthracis polyglutamate capsule synthesis. J Bacteriol 187:7765–7772 http://dx.doi.org/10.1128/JB.187.22.7765-7772.2005. [PubMed]
318. Dai Z, Sirard JC, Mock M, Koehler TM. 1995. The atxA gene product activates transcription of the anthrax toxin genes and is essential for virulence. Mol Microbiol 16:1171–1181 http://dx.doi.org/10.1111/j.1365-2958.1995.tb02340.x. [PubMed]
319. Dale JL, Raynor MJ, Dwivedi P, Koehler TM. 2012. cis-Acting elements that control expression of the master virulence regulatory gene atxA in Bacillus anthracis. J Bacteriol 194:4069–4079 http://dx.doi.org/10.1128/JB.00776-12. [PubMed]
320. Dale JL, Raynor MJ, Ty MC, Hadjifrangiskou M, Koehler TM. 2018. A dual role for the Bacillus anthracis master virulence regulator AtxA: control of sporulation and anthrax toxin production. Front Microbiol 9:482 http://dx.doi.org/10.3389/fmicb.2018.00482. [PubMed]
321. Drysdale M, Bourgogne A, Hilsenbeck SG, Koehler TM. 2004. atxA controls Bacillus anthracis capsule synthesis via acpA and a newly discovered regulator, acpB. J Bacteriol 186:307–315 http://dx.doi.org/10.1128/JB.186.2.307-315.2004. [PubMed]
322. Vietri NJ, Marrero R, Hoover TA, Welkos SL. 1995. Identification and characterization of a trans-activator involved in the regulation of encapsulation by Bacillus anthracis. Gene 152:1–9 http://dx.doi.org/10.1016/0378-1119(94)00662-C.
323. Drysdale M, Bourgogne A, Koehler TM. 2005. Transcriptional analysis of the Bacillus anthracis capsule regulators. J Bacteriol 187:5108–5114 http://dx.doi.org/10.1128/JB.187.15.5108-5114.2005. [PubMed]
324. Drysdale M, Heninger S, Hutt J, Chen Y, Lyons CR, Koehler TM. 2005. Capsule synthesis by Bacillus anthracis is required for dissemination in murine inhalation anthrax. EMBO J 24:221–227 http://dx.doi.org/10.1038/sj.emboj.7600495. [PubMed]
325. Chiang C, Bongiorni C, Perego M. 2011. Glucose-dependent activation of Bacillus anthracis toxin gene expression and virulence requires the carbon catabolite protein CcpA. J Bacteriol 193:52–62 http://dx.doi.org/10.1128/JB.01656-09. [PubMed]
326. Wilson AC, Hoch JA, Perego M. 2009. Two small c-type cytochromes affect virulence gene expression in Bacillus anthracis. Mol Microbiol 72:109–123 http://dx.doi.org/10.1111/j.1365-2958.2009.06627.x. [PubMed]
327. Dai Z, Koehler TM. 1997. Regulation of anthrax toxin activator gene ( atxA) expression in Bacillus anthracis: temperature, not CO2/bicarbonate, affects AtxA synthesis. Infect Immun 65:2576–2582.
328. van Schaik W, Prigent J, Fouet A. 2007. The stringent response of Bacillus anthracis contributes to sporulation but not to virulence. Microbiology 153:4234–4239 http://dx.doi.org/10.1099/mic.0.2007/010355-0. [PubMed]
329. Strauch MA, Ballar P, Rowshan AJ, Zoller KL. 2005. The DNA-binding specificity of the Bacillus anthracis AbrB protein. Microbiology 151:1751–1759 http://dx.doi.org/10.1099/mic.0.27803-0. [PubMed]
330. Tsvetanova B, Wilson AC, Bongiorni C, Chiang C, Hoch JA, Perego M. 2007. Opposing effects of histidine phosphorylation regulate the AtxA virulence transcription factor in Bacillus anthracis. Mol Microbiol 63:644–655 http://dx.doi.org/10.1111/j.1365-2958.2006.05543.x. [PubMed]
331. Hammerstrom TG, Roh JH, Nikonowicz EP, Koehler TM. 2011. Bacillus anthracis virulence regulator AtxA: oligomeric state, function and CO(2)-signalling. Mol Microbiol 82:634–647 http://dx.doi.org/10.1111/j.1365-2958.2011.07843.x. [PubMed]
332. Hondorp ER, Hou SC, Hause LL, Gera K, Lee CE, McIver KS. 2013. PTS phosphorylation of Mga modulates regulon expression and virulence in the group A streptococcus. Mol Microbiol 88:1176–1193 http://dx.doi.org/10.1111/mmi.12250. [PubMed]
333. Hammerstrom TG, Horton LB, Swick MC, Joachimiak A, Osipiuk J, Koehler TM. 2015. Crystal structure of Bacillus anthracis virulence regulator AtxA and effects of phosphorylated histidines on multimerization and activity. Mol Microbiol 95:426–441 http://dx.doi.org/10.1111/mmi.12867. [PubMed]
334. Kolstø AB, Tourasse NJ, Økstad OA. 2009. What sets Bacillus anthracis apart from other Bacillus species? Annu Rev Microbiol 63:451–476 http://dx.doi.org/10.1146/annurev.micro.091208.073255. [PubMed]
335. Timmery S, Modrie P, Minet O, Mahillon J. 2009. Plasmid capture by the Bacillus thuringiensis conjugative plasmid pXO16. J Bacteriol 191:2197–2205 http://dx.doi.org/10.1128/JB.01700-08. [PubMed]
336. Andrup L, Jørgensen O, Wilcks A, Smidt L, Jensen GB. 1996. Mobilization of “nonmobilizable” plasmids by the aggregation-mediated conjugation system of Bacillus thuringiensis. Plasmid 36:75–85 http://dx.doi.org/10.1006/plas.1996.0035. [PubMed]
337. Wilcks A, Jayaswal N, Lereclus D, Andrup L. 1998. Characterization of plasmid pAW63, a second self-transmissible plasmid in Bacillus thuringiensis subsp. kurstaki HD73. Microbiology 144:1263–1270 http://dx.doi.org/10.1099/00221287-144-5-1263. [PubMed]
338. Thorne CB. 1993. Bacillus anthracis, p 113–124. In Sonenshein AL, Hoch JA, Losick R (ed), Bacillus subtilis and Other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular Genetics. American Society for Microbiology, Washington, DC.
339. Thorne CB. 1968. Transducing bacteriophage for Bacillus cereus. J Virol 2:657–662.
340. Lecadet MM, Blondel MO, Ribier J. 1980. Generalized transduction in Bacillus thuringiensis var. berliner 1715 using bacteriophage CP-54Ber. J Gen Microbiol 121:203–212. [PubMed]
341. Thorne CB. 1978. Transduction in Bacillus thuringiensis. Appl Environ Microbiol 35:1109–1115.
342. Lecadet MM, Chaufaux J, Ribier J, Lereclus D. 1992. Construction of novel Bacillus thuringiensis strains with different insecticidal activities by transduction and transformation. Appl Environ Microbiol 58:840–849.
343. Battisti L, Green BD, Thorne CB. 1985. Mating system for transfer of plasmids among Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis. J Bacteriol 162:543–550.
344. Barsomian GD, Robillard NJ, Thorne CB. 1984. Chromosomal mapping of Bacillus thuringiensis by transduction. J Bacteriol 157:746–750.
345. Lereclus D, Menou G, Lecadet M-M. 1983. Isolation of a DNA sequence related to several plasmids from Bacillus thuringiensis after a mating involving the Streptococcus faecalis plasmid pAM beta 1. Mol Gen Genet 191:307–313 http://dx.doi.org/10.1007/BF00334831.
346. Lereclus D, Mahillon J, Menou G, Lecadet M-M. 1986. Identification of Tn 4430, a transposon of Bacillus thuringiensis functional in Escherichia coli. Mol Gen Genet 204:52–57 http://dx.doi.org/10.1007/BF00330186.
347. Yuan Y, Zheng D, Hu X, Cai Q, Yuan Z. 2010. Conjugative transfer of insecticidal plasmid pHT73 from Bacillus thuringiensis to B. anthracis and compatibility of this plasmid with pXO1 and pXO2. Appl Environ Microbiol 76:468–473 http://dx.doi.org/10.1128/AEM.01984-09. [PubMed]
348. Reddy A, Battisti L, Thorne CB. 1987. Identification of self-transmissible plasmids in four Bacillus thuringiensis subspecies. J Bacteriol 169:5263–5270 http://dx.doi.org/10.1128/jb.169.11.5263-5270.1987. [PubMed]
349. Jarrett P, Stephenson M. 1990. Plasmid transfer between strains of Bacillus thuringiensis infecting Galleria mellonella and Spodoptera littoralis. Appl Environ Microbiol 56:1608–1614.
350. Vilas-Bôas G, Vilas-Bôas LA, Lereclus D, Arantes O. 1998. Bacillus thuringiensis conjugation under environmental conditions. FEMS Microbiol Ecol 25:369–374 http://dx.doi.org/10.1016/S0168-6496(98)00005-1.
351. Thomas DJ, Morgan JA, Whipps JM, Saunders JR. 2000. Plasmid transfer between the Bacillus thuringiensis subspecies kurstaki and tenebrionis in laboratory culture and soil and in lepidopteran and coleopteran larvae. Appl Environ Microbiol 66:118–124 http://dx.doi.org/10.1128/AEM.66.1.118-124.2000. [PubMed]
352. Wilcks A, Smidt L, Bahl MI, Hansen BM, Andrup L, Hendriksen NB, Licht TR. 2008. Germination and conjugation of Bacillus thuringiensis subsp. israelensis in the intestine of gnotobiotic rats. J Appl Microbiol 104:1252–1259 http://dx.doi.org/10.1111/j.1365-2672.2007.03657.x. [PubMed]
353. Thomas DJ, Morgan JA, Whipps JM, Saunders JR. 2001. Plasmid transfer between Bacillus thuringiensis subsp. israelensis strains in laboratory culture, river water, and dipteran larvae. Appl Environ Microbiol 67:330–338 http://dx.doi.org/10.1128/AEM.67.1.330-338.2001. [PubMed]
354. Modrie P, Beuls E, Mahillon J. 2010. Differential transfer dynamics of pAW63 plasmid among members of the Bacillus cereus group in food microcosms. J Appl Microbiol 108:888–897 http://dx.doi.org/10.1111/j.1365-2672.2009.04488.x. [PubMed]
355. Van der Auwera GA, Timmery S, Hoton F, Mahillon J. 2007. Plasmid exchanges among members of the Bacillus cereus group in foodstuffs. Int J Food Microbiol 113:164–172 http://dx.doi.org/10.1016/j.ijfoodmicro.2006.06.030. [PubMed]
356. Hu X, Van der Auwera G, Timmery S, Zhu L, Mahillon J. 2009. Distribution, diversity, and potential mobility of extrachromosomal elements related to the Bacillus anthracis pXO1 and pXO2 virulence plasmids. Appl Environ Microbiol 75:3016–3028 http://dx.doi.org/10.1128/AEM.02709-08. [PubMed]
357. Pannucci J, Okinaka RT, Sabin R, Kuske CR. 2002. Bacillus anthracis pXO1 plasmid sequence conservation among closely related bacterial species. J Bacteriol 184:134–141 http://dx.doi.org/10.1128/JB.184.1.134-141.2002. [PubMed]
358. Hoffmaster AR, Hill KK, Gee JE, Marston CK, De BK, Popovic T, Sue D, Wilkins PP, Avashia SB, Drumgoole R, Helma CH, Ticknor LO, Okinaka RT, Jackson PJ. 2006. Characterization of Bacillus cereus isolates associated with fatal pneumonias: strains are closely related to Bacillus anthracis and harbor B. anthracis virulence genes. J Clin Microbiol 44:3352–3360 http://dx.doi.org/10.1128/JCM.00561-06. [PubMed]
359. Hernandez E, Ramisse F, Ducoureau JP, Cruel T, Cavallo JD. 1998. Bacillus thuringiensis subsp. konkukian (serotype H34) superinfection: case report and experimental evidence of pathogenicity in immunosuppressed mice. J Clin Microbiol 36:2138–2139.
360. Van der Auwera GA, Timmery S, Mahillon J. 2008. Self-transfer and mobilisation capabilities of the pXO2-like plasmid pBT9727 from Bacillus thuringiensis subsp. konkukian 97-27. Plasmid 59:134–138 http://dx.doi.org/10.1016/j.plasmid.2007.11.007. [PubMed]
361. Koehler TM, Thorne CB. 1987. Bacillus subtilis (natto) plasmid pLS20 mediates interspecies plasmid transfer. J Bacteriol 169:5271–5278 http://dx.doi.org/10.1128/jb.169.11.5271-5278.1987. [PubMed]
362. DeWitt T, Grossman AD. 2014. The bifunctional cell wall hydrolase CwlT is needed for conjugation of the integrative and conjugative element ICEBs1 in Bacillus subtilis and B. anthracis. J Bacteriol 196:1588–1596 http://dx.doi.org/10.1128/JB.00012-14. [PubMed]
363. Zhang J, Hodgman TC, Krieger L, Schnetter W, Schairer HU. 1997. Cloning and analysis of the first cry gene from Bacillus popilliae. J Bacteriol 179:4336–4341 http://dx.doi.org/10.1128/jb.179.13.4336-4341.1997. [PubMed]
364. Qureshi N, Chawla S, Likitvivatanavong S, Lee HL, Gill SS. 2014. The cry toxin operon of Clostridium bifermentans subsp. malaysia is highly toxic to Aedes larval mosquitoes. Appl Environ Microbiol 80:5689–5697 http://dx.doi.org/10.1128/AEM.01139-14. [PubMed]
365. Bone EJ, Ellar DJ. 1989. Transformation of Bacillus thuringiensis by electroporation. FEMS Microbiol Lett 49:171–177 http://dx.doi.org/10.1111/j.1574-6968.1989.tb03039.x.
366. Lereclus D, Arantes O, Chaufaux J, Lecadet M. 1989. Transformation and expression of a cloned delta-endotoxin gene in Bacillus thuringiensis. FEMS Microbiol Lett 51:211–217.
367. Schurter W, Geiser M, Mathé D. 1989. Efficient transformation of Bacillus thuringiensis and B. cereus via electroporation: transformation of acrystalliferous strains with a cloned delta-endotoxin gene. Mol Gen Genet 218:177–181 http://dx.doi.org/10.1007/BF00330581.
368. Pezard C, Berche P, Mock M. 1991. Contribution of individual toxin components to virulence of Bacillus anthracis. Infect Immun 59:3472–3477.
369. Sirard JC, Mock M, Fouet A. 1994. The three Bacillus anthracis toxin genes are coordinately regulated by bicarbonate and temperature. J Bacteriol 176:5188–5192 http://dx.doi.org/10.1128/jb.176.16.5188-5192.1994. [PubMed]
370. Dommel MK, Frenzel E, Strasser B, Blöchinger C, Scherer S, Ehling-Schulz M. 2010. Identification of the main promoter directing cereulide biosynthesis in emetic Bacillus cereus and its application for real-time monitoring of ces gene expression in foods. Appl Environ Microbiol 76:1232–1240 http://dx.doi.org/10.1128/AEM.02317-09. [PubMed]
371. Macaluso A, Mettus AM. 1991. Efficient transformation of Bacillus thuringiensis requires nonmethylated plasmid DNA. J Bacteriol 173:1353–1356 http://dx.doi.org/10.1128/jb.173.3.1353-1356.1991. [PubMed]
372. Marrero R, Welkos SL. 1995. The transformation frequency of plasmids into Bacillus anthracis is affected by adenine methylation. Gene 152:75–78 http://dx.doi.org/10.1016/0378-1119(94)00647-B.
373. Trieu-Cuot P, Carlier C, Martin P, Courvalin P. 1987. Plasmid transfer by conjugation from Escherichia coli to Gram-positive bacteria. FEMS Microbiol Lett 48:289–294 http://dx.doi.org/10.1111/j.1574-6968.1987.tb02558.x.
374. Arantes O, Lereclus D. 1991. Construction of cloning vectors for Bacillus thuringiensis. Gene 108:115–119 http://dx.doi.org/10.1016/0378-1119(91)90495-W.
375. Arnaud M, Chastanet A, Débarbouillé M. 2004. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, Gram-positive bacteria. Appl Environ Microbiol 70:6887–6891 http://dx.doi.org/10.1128/AEM.70.11.6887-6891.2004. [PubMed]
376. Saldanha RJ, Pemberton A, Shiflett P, Perutka J, Whitt JT, Ellington A, Lambowitz AM, Kramer R, Taylor D, Lamkin TJ. 2013. Rapid targeted gene disruption in Bacillus anthracis. BMC Biotechnol 13:72 http://dx.doi.org/10.1186/1472-6750-13-72. [PubMed]
377. Pomerantsev AP, McCall RM, Chahoud M, Hepler NK, Fattah R, Leppla SH. 2017. Genome engineering in Bacillus anthracis using tyrosine site-specific recombinases. PLoS One 12:e0183346 http://dx.doi.org/10.1371/journal.pone.0183346. [PubMed]
378. Janes BK, Stibitz S. 2006. Routine markerless gene replacement in Bacillus anthracis. Infect Immun 74:1949–1953 http://dx.doi.org/10.1128/IAI.74.3.1949-1953.2006. [PubMed]
379. Plaut RD, Stibitz S. 2015. Improvements to a markerless allelic exchange system for Bacillus anthracis. PLoS One 10:e0142758 http://dx.doi.org/10.1371/journal.pone.0142758. [PubMed]
380. Lee JY, Janes BK, Passalacqua KD, Pfleger BF, Bergman NH, Liu H, Håkansson K, Somu RV, Aldrich CC, Cendrowski S, Hanna PC, Sherman DH. 2007. Biosynthetic analysis of the petrobactin siderophore pathway from Bacillus anthracis. J Bacteriol 189:1698–1710 http://dx.doi.org/10.1128/JB.01526-06. [PubMed]
381. Vörös A, Simm R, Slamti L, McKay MJ, Hegna IK, Nielsen-LeRoux C, Hassan KA, Paulsen IT, Lereclus D, Økstad OA, Molloy MP, Kolstø AB. 2014. SecDF as part of the Sec-translocase facilitates efficient secretion of Bacillus cereus toxins and cell wall-associated proteins. PLoS One 9:e103326 http://dx.doi.org/10.1371/journal.pone.0103326. [PubMed]
382. Simm R, Vörös A, Ekman JV, Sødring M, Nes I, Kroeger JK, Saidijam M, Bettaney KE, Henderson PJ, Salkinoja-Salonen M, Kolstø AB. 2012. BC4707 is a major facilitator superfamily multidrug resistance transport protein from Bacillus cereus implicated in fluoroquinolone tolerance. PLoS One 7:e36720 http://dx.doi.org/10.1371/journal.pone.0036720. [PubMed]
383. Klimowicz AK, Benson TA, Handelsman J. 2010. A quadruple-enterotoxin-deficient mutant of Bacillus thuringiensis remains insecticidal. Microbiology 156:3575–3583 http://dx.doi.org/10.1099/mic.0.039925-0. [PubMed]
384. Gominet M, Slamti L, Gilois N, Rose M, Lereclus D. 2001. Oligopeptide permease is required for expression of the Bacillus thuringiensis plcR regulon and for virulence. Mol Microbiol 40:963–975 http://dx.doi.org/10.1046/j.1365-2958.2001.02440.x. [PubMed]
385. Espinasse S, Gohar M, Lereclus D, Sanchis V. 2002. An ABC transporter from Bacillus thuringiensis is essential for beta-exotoxin I production. J Bacteriol 184:5848–5854 http://dx.doi.org/10.1128/JB.184.21.5848-5854.2002. [PubMed]
386. Fedhila S, Guillemet E, Nel P, Lereclus D. 2004. Characterization of two Bacillus thuringiensis genes identified by in vivo screening of virulence factors. Appl Environ Microbiol 70:4784–4791 http://dx.doi.org/10.1128/AEM.70.8.4784-4791.2004. [PubMed]
387. Tam C, Glass EM, Anderson DM, Missiakas D. 2006. Transposon mutagenesis of Bacillus anthracis strain Sterne using Bursa aurealis. Plasmid 56:74–77 http://dx.doi.org/10.1016/j.plasmid.2006.01.002. [PubMed]
388. McGillivray SM, Ebrahimi CM, Fisher N, Sabet M, Zhang DX, Chen Y, Haste NM, Aroian RV, Gallo RL, Guiney DG, Friedlander AM, Koehler TM, Nizet V. 2009. ClpX contributes to innate defense peptide resistance and virulence phenotypes of Bacillus anthracis. J Innate Immun 1:494–506 http://dx.doi.org/10.1159/000225955. [PubMed]
389. Ivins BE, Welkos SL, Knudson GB, Leblanc DJ. 1988. Transposon Tn916 mutagenesis in Bacillus anthracis. Infect Immun 56:176–181.
390. Hoffmaster AR, Koehler TM. 1997. The anthrax toxin activator gene atxA is associated with CO2-enhanced non-toxin gene expression in Bacillus anthracis. Infect Immun 65:3091–3099.
391. Song F, Peng Q, Brillard J, Buisson C, de Been M, Abee T, Broussolle V, Huang D, Zhang J, Lereclus D, Nielsen-LeRoux C. 2012. A multicomponent sugar phosphate sensor system specifically induced in Bacillus cereus during infection of the insect gut. FASEB J 26:3336–3350 http://dx.doi.org/10.1096/fj.11-197681. [PubMed]
392. Passalacqua KD, Bergman NH, Lee JY, Sherman DH, Hanna PC. 2007. The global transcriptional responses of Bacillus anthracis Sterne (34F2) and a Delta sodA1 mutant to paraquat reveal metal ion homeostasis imbalances during endogenous superoxide stress. J Bacteriol 189:3996–4013 http://dx.doi.org/10.1128/JB.00185-07. [PubMed]
393. Passalacqua KD, Varadarajan A, Byrd B, Bergman NH. 2009. Comparative transcriptional profiling of Bacillus cereus sensu lato strains during growth in CO 2-bicarbonate and aerobic atmospheres. PLoS One 4:e4904 http://dx.doi.org/10.1371/journal.pone.0004904. [PubMed]
394. Martin J, Zhu W, Passalacqua KD, Bergman N, Borodovsky M. 2010. Bacillus anthracis genome organization in light of whole transcriptome sequencing. BMC Bioinformatics 11(Suppl 3) :S10 http://dx.doi.org/10.1186/1471-2105-11-S3-S10. [PubMed]
395. Mols M, Mastwijk H, Nierop Groot M, Abee T. 2013. Physiological and transcriptional response of Bacillus cereus treated with low-temperature nitrogen gas plasma. J Appl Microbiol 115:689–702 http://dx.doi.org/10.1111/jam.12278. [PubMed]
396. Agaisse H, Lereclus D. 1994. Structural and functional analysis of the promoter region involved in full expression of the cryIIIA toxin gene of Bacillus thuringiensis. Mol Microbiol 13:97–107 http://dx.doi.org/10.1111/j.1365-2958.1994.tb00405.x. [PubMed]
397. Bartkus JM, Leppla SH. 1989. Transcriptional regulation of the protective antigen gene of Bacillus anthracis. Infect Immun 57:2295–2300.
398. Han H, Wilson AC. 2013. The two CcdA proteins of Bacillus anthracis differentially affect virulence gene expression and sporulation. J Bacteriol 195:5242–5249 http://dx.doi.org/10.1128/JB.00917-13. [PubMed]
399. Ben Rejeb S, Lereclus D, Slamti L. 2017. Analysis of abrB expression during the infectious cycle of Bacillus thuringiensis reveals population heterogeneity. Front Microbiol 8:2471 http://dx.doi.org/10.3389/fmicb.2017.02471. [PubMed]
400. Dunn AK, Handelsman J. 1999. A vector for promoter trapping in Bacillus cereus. Gene 226:297–305 http://dx.doi.org/10.1016/S0378-1119(98)00544-7.
401. Turnbull PC, Sirianni NM, LeBron CI, Samaan MN, Sutton FN, Reyes AE, Peruski LF Jr. 2004. MICs of selected antibiotics for Bacillus anthracis, Bacillus cereus, Bacillus thuringiensis, and Bacillus mycoides from a range of clinical and environmental sources as determined by the Etest. J Clin Microbiol 42:3626–3634 http://dx.doi.org/10.1128/JCM.42.8.3626-3634.2004. [PubMed]
402. Weber DJ, Rutala WA. 1988. Bacillus species. Infect Control Hosp Epidemiol 9:368–373 http://dx.doi.org/10.2307/30145465. [PubMed]
403. Chen Y, Succi J, Tenover FC, Koehler TM. 2003. Beta-lactamase genes of the penicillin-susceptible Bacillus anthracis Sterne strain. J Bacteriol 185:823–830 http://dx.doi.org/10.1128/JB.185.3.823-830.2003. [PubMed]
404. Inglesby TV, O’Toole T, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, Friedlander AM, Gerberding J, Hauer J, Hughes J, McDade J, Osterholm MT, Parker G, Perl TM, Russell PK, Tonat K, Working Group on Civilian Biodefense. 2002. Anthrax as a biological weapon, 2002: updated recommendations for management. JAMA 287:2236–2252 http://dx.doi.org/10.1001/jama.287.17.2236. [PubMed]
405. Hendricks KA, Wright ME, Shadomy SV, Bradley JS, Morrow MG, Pavia AT, Rubinstein E, Holty JE, Messonnier NE, Smith TL, Pesik N, Treadwell TA, Bower WA, Workgroup on Anthrax Clinical Guidelines. 2014. Centers for disease control and prevention expert panel meetings on prevention and treatment of anthrax in adults. Emerg Infect Dis 20:20 http://dx.doi.org/10.3201/eid2002.130687. [PubMed]
406. Bast DJ, Athamna A, Duncan CL, de Azavedo JC, Low DE, Rahav G, Farrell D, Rubinstein E. 2004. Type II topoisomerase mutations in Bacillus anthracis associated with high-level fluoroquinolone resistance. J Antimicrob Chemother 54:90–94 http://dx.doi.org/10.1093/jac/dkh294. [PubMed]
407. Price LB, Vogler A, Pearson T, Busch JD, Schupp JM, Keim P. 2003. In vitro selection and characterization of Bacillus anthracis mutants with high-level resistance to ciprofloxacin. Antimicrob Agents Chemother 47:2362–2365 http://dx.doi.org/10.1128/AAC.47.7.2362-2365.2003. [PubMed]
408. Kalns J, Morris J, Eggers J, Kiel J. 2002. Delayed treatment with doxycycline has limited effect on anthrax infection in BLK57/B6 mice. Biochem Biophys Res Commun 297:506–509 http://dx.doi.org/10.1016/S0006-291X(02)02226-X.
409. Peterson JW, Moen ST, Healy D, Pawlik JE, Taormina J, Hardcastle J, Thomas JM, Lawrence WS, Ponce C, Chatuev BM, Gnade BT, Foltz SM, Agar SL, Sha J, Klimpel GR, Kirtley ML, Eaves-Pyles T, Chopra AK. 2010. Protection afforded by fluoroquinolones in animal models of respiratory infections with Bacillus anthracis, Yersinia pestis, and Francisella tularensis. Open Microbiol J 4:34–46 http://dx.doi.org/10.2174/1874285801004010034. [PubMed]
410. Holty JE, Kim RY, Bravata DM. 2006. Anthrax: a systematic review of atypical presentations. Ann Emerg Med 48:200–211 http://dx.doi.org/10.1016/j.annemergmed.2005.11.035. [PubMed]
411. Jernigan JA, Stephens DS, Ashford DA, Omenaca C, Topiel MS, Galbraith M, Tapper M, Fisk TL, Zaki S, Popovic T, Meyer RF, Quinn CP, Harper SA, Fridkin SK, Sejvar JJ, Shepard CW, McConnell M, Guarner J, Shieh WJ, Malecki JM, Gerberding JL, Hughes JM, Perkins BA, Anthrax Bioterrorism Investigation Team. 2001. Bioterrorism-related inhalational anthrax: the first 10 cases reported in the United States. Emerg Infect Dis 7:933–944 http://dx.doi.org/10.3201/eid0706.010604. [PubMed]
412. Mourez M, Kane RS, Mogridge J, Metallo S, Deschatelets P, Sellman BR, Whitesides GM, Collier RJ. 2001. Designing a polyvalent inhibitor of anthrax toxin. Nat Biotechnol 19:958–961 http://dx.doi.org/10.1038/nbt1001-958. [PubMed]
413. Hull AK, Criscuolo CJ, Mett V, Groen H, Steeman W, Westra H, Chapman G, Legutki B, Baillie L, Yusibov V. 2005. Human-derived, plant-produced monoclonal antibody for the treatment of anthrax. Vaccine 23:2082–2086 http://dx.doi.org/10.1016/j.vaccine.2005.01.013. [PubMed]
414. Ionin B, Hopkins RJ, Pleune B, Sivko GS, Reid FM, Clement KH, Rudge TL Jr, Stark GV, Innes A, Sari S, Guina T, Howard C, Smith J, Swoboda ML, Vert-Wong E, Johnson V, Nabors GS, Skiadopoulos MH. 2013. Evaluation of immunogenicity and efficacy of anthrax vaccine adsorbed for postexposure prophylaxis. Clin Vaccine Immunol 20:1016–1026 http://dx.doi.org/10.1128/CVI.00099-13. [PubMed]
415. Chen L, Schiffer JM, Dalton S, Sabourin CL, Niemuth NA, Plikaytis BD, Quinn CP. 2014. Comprehensive analysis and selection of anthrax vaccine adsorbed immune correlates of protection in rhesus macaques. Clin Vaccine Immunol 21:1512–1520 http://dx.doi.org/10.1128/CVI.00469-14. [PubMed]
416. Little SF, Ivins BE, Webster WM, Fellows PF, Pitt ML, Norris SL, Andrews GP. 2006. Duration of protection of rabbits after vaccination with Bacillus anthracis recombinant protective antigen vaccine. Vaccine 24:2530–2536 http://dx.doi.org/10.1016/j.vaccine.2005.12.028. [PubMed]
417. Larkin M. 2002. Anthrax vaccine is safe and effective-but needs improvement, says IOM. Lancet 359:951 http://dx.doi.org/10.1016/S0140-6736(02)08051-0.
418. Fay MP, Follmann DA, Lynn F, Schiffer JM, Stark GV, Kohberger R, Quinn CP, Nuzum EO. 2012. Anthrax vaccine-induced antibodies provide cross-species prediction of survival to aerosol challenge. Sci Transl Med 4:151ra126 http://dx.doi.org/10.1126/scitranslmed.3004073. [PubMed]
419. Sivko GS, Stark GV, Tordoff KP, Taylor KL, Glaze E, VanRaden M, Schiffer JM, Hewitt JA, Quinn CP, Nuzum EO. 2016. Evaluation of early immune response-survival relationship in cynomolgus macaques after Anthrax Vaccine Adsorbed vaccination and Bacillus anthracis spore challenge. Vaccine 34:6518–6528 http://dx.doi.org/10.1016/j.vaccine.2016.04.048. [PubMed]
420. Dumas EK, Gross T, Larabee J, Pate L, Cuthbertson H, Charlton S, Hallis B, Engler RJM, Collins LC Jr, Spooner CE, Chen H, Ballard J, James JA, Farris AD. 2017. Anthrax vaccine precipitated induces edema toxin-neutralizing, edema factor-specific antibodies in human recipients. Clin Vaccine Immunol 24:24 http://dx.doi.org/10.1128/CVI.00165-17. [PubMed]
421. Dumas EK, Garman L, Cuthbertson H, Charlton S, Hallis B, Engler RJM, Choudhari S, Picking WD, James JA, Farris AD. 2017. Lethal factor antibodies contribute to lethal toxin neutralization in recipients of anthrax vaccine precipitated. Vaccine 35:3416–3422 http://dx.doi.org/10.1016/j.vaccine.2017.05.006. [PubMed]
422. Zegers ND, Kluter E, van Der Stap H, van Dura E, van Dalen P, Shaw M, Baillie L. 1999. Expression of the protective antigen of Bacillus anthracis by Lactobacillus casei: towards the development of an oral vaccine against anthrax. J Appl Microbiol 87:309–314 http://dx.doi.org/10.1046/j.1365-2672.1999.00900.x. [PubMed]
423. Garmory HS, Titball RW, Griffin KF, Hahn U, Böhm R, Beyer W. 2003. Salmonella enterica serovar Typhimurium expressing a chromosomally integrated copy of the Bacillus anthracis protective antigen gene protects mice against an anthrax spore challenge. Infect Immun 71:3831–3836 http://dx.doi.org/10.1128/IAI.71.7.3831-3836.2003. [PubMed]
424. Galloway DR, Baillie L. 2004. DNA vaccines against anthrax. Expert Opin Biol Ther 4:1661–1667 http://dx.doi.org/10.1517/14712598.4.10.1661. [PubMed]
425. Price BM, Liner AL, Park S, Leppla SH, Mateczun A, Galloway DR. 2001. Protection against anthrax lethal toxin challenge by genetic immunization with a plasmid encoding the lethal factor protein. Infect Immun 69:4509–4515 http://dx.doi.org/10.1128/IAI.69.7.4509-4515.2001. [PubMed]
426. Schneerson R, Kubler-Kielb J, Liu TY, Dai ZD, Leppla SH, Yergey A, Backlund P, Shiloach J, Majadly F, Robbins JB. 2003. Poly(gamma- d-glutamic acid) protein conjugates induce IgG antibodies in mice to the capsule of Bacillus anthracis: a potential addition to the anthrax vaccine. Proc Natl Acad Sci U S A 100:8945–8950 http://dx.doi.org/10.1073/pnas.1633512100. [PubMed]
427. Jones RM, Burke M, Dubose D, Chichester JA, Manceva S, Horsey A, Streatfield SJ, Breit J, Yusibov V. 2017. Stability and pre-formulation development of a plant-produced anthrax vaccine candidate. Vaccine 35:5463–5470 http://dx.doi.org/10.1016/j.vaccine.2016.12.009. [PubMed]
428. Sterne M. 1946. Avirulent anthrax vaccine. Onderstepoort J Vet Sci Anim Ind 21:41–43.
429. EFSA Panel on Biological Hazards. 2016. Risks for public health related to the presence of Bacillus cereus and other Bacillus spp. including Bacillus thuringiensis in foodstuffs. EFSA J. https://doi.org/10.2903/j.efsa.2016.4524.
430. Guinebretière MH, Thompson FL, Sorokin A, Normand P, Dawyndt P, Ehling-Schulz M, Svensson B, Sanchis V, Nguyen-The C, Heyndrickx M, De Vos P. 2008. Ecological diversification in the Bacillus cereus group. Environ Microbiol 10:851–865 http://dx.doi.org/10.1111/j.1462-2920.2007.01495.x. [PubMed]
431. Méric G, Mageiros L, Pascoe B, Woodcock DJ, Mourkas E, Lamble S, Bowden R, Jolley KA, Raymond B, Sheppard SK. 2018. Lineage-specific plasmid acquisition and the evolution of specialized pathogens in Bacillus thuringiensis and the Bacillus cereus group. Mol Ecol 27:1524–1540 http://dx.doi.org/10.1111/mec.14546. [PubMed]
432. Margolis PS, Driks A, Losick R. 1993. Sporulation gene spoIIB from Bacillus subtilis. J Bacteriol 175:528–540 http://dx.doi.org/10.1128/jb.175.2.528. [PubMed]
433. Slamti L, Lemy C, Henry C, Guillot A, Huillet E, Lereclus D 2016. CodY Regulates the Activity of the Virulence Quorum Sensor PlcR by Controlling the Import of the Signaling Peptide PapR in Bacillus thuringiensis. Front Microbiol 6:1501 https://doi.org/10.3389/fmicb.2015.01501. [PubMed]
434. Mahillon J, Chungjatupornchai W, Decock J, Dierickx S, Michiels F, Peferoen M, Joos H. 1989. Transformation of Bacillus thuringiensis by electroporation. FEMS Microbiol Lett 60:205–210 https://doi.org/10.1111/j.1574-6968.1989.tb03447.x.
435. Lereclus D, Arantes O. 1992. spbA locus ensures the segregational stability of pHT1030, a novel type of Gram-positive replicon. Mol. Microbiol 7:35–36 https://doi.org/10.1111/j.1365-2958.1992.tb00835.x. [PubMed]
436. Lereclus D, Vallade M, Chaufaux J, Arantes O, Rambaud S. 1992. Expansion of insecticidal host range of Bacillus thuringiensis by in vivo genetic recombination. Biotechnology (N Y) 10:418–21 http://dx.doi.org/10.1038/nbt0492-418. [PubMed]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.GPP3-0032-2018
2019-05-17
2019-06-19

Abstract:

The group includes several species with closely related phylogeny. The most well-studied members of the group, , , and , are known for their pathogenic potential. Here, we present the historical rationale for speciation and discuss shared and unique features of these bacteria. Aspects of cell morphology and physiology, and genome sequence similarity and gene synteny support close evolutionary relationships for these three species. For many strains, distinct differences in virulence factor synthesis provide facile means for species assignment. is the causative agent of anthrax. Some strains are commonly recognized as food poisoning agents, but strains can also cause localized wound and eye infections as well as systemic disease. Certain strains are entomopathogens and have been commercialized for use as biopesticides, while some strains have been reported to cause infection in immunocompromised individuals. In this article we compare and contrast , , and , including ecology, cell structure and development, virulence attributes, gene regulation and genetic exchange systems, and experimental models of disease.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

The five major phylogenetic clades of the group. Clade I is known as the clade but also includes emetic and several clinical isolates. Clade II is known as the / clade and includes most of the commercially used as well as the and type strains. Clade III is known as the clade and comprises most of the psychrotolerant isolates of the group. Clade IV includes strains belonging to various group species. These clades are based on multilocus sequence typing, amplified fragment length polymorphism, and whole-genome sequence data ( 429 431 ). The thermotolerant strains belonging to the species cluster together in a separate group.

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0032-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Transmission of the group species from the soil reservoir to humans via food and textile production. Soil and soil-associated organisms including plants, insects, nematodes, and amoebae, serve as the major reservoirs for acquisition of spores. The bacteria are transferred to humans through agricultural products including food and animal-associated textiles, entering humans and other mammals through ingestion, inhalation, and breaks in the skin. Illustration credit: Olive E. Morrison.

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0032-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Thin-section transmission electron micrograph of cell after 5 hours of sporulation (left image) and a mature spore (right image). The forespore inner membrane (FS IM) and nascent exosporium (Ex) (left image), and forespore inner membrane (FS IM), mature exosporium (Ex), coat (Ct), interspace, (Is), and cortex (Cx) (right image) are labeled. sporulating cell with parasporal crystal. Cells were sporulated, prepared, and imaged as described in reference 432 . Image credit: (A) Tyler Boone and Adam Driks. (B) Fuping Song.

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0032-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4
FIGURE 4

Cereulide, the emetic toxin of .

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0032-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5
FIGURE 5

The infectious cycle of in a susceptible insect larva. Ingestion of spores and crystals is followed by the dissolution of the crystal in the alkaline environment of the midgut. Insect proteases activate Cry proteins. Spores germinate in the paralyzed insect gut. Cry toxins degrade the peritrophic membrane. Bacteria multiply and express PlcR-regulated genes. The intestinal barrier is disrupted and bacteria gain access to the hemocoel. The bacteria resist host defenses and cause a fatal septicemia. The NprR regulon is activated, and the bacteria survive in the host cadaver. Finally, spores and vegetative cells are disseminated outside of the host.

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0032-2018
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Generic image for table
TABLE 1

Exotoxins, the major virulence factors of the group

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0032-2018

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error