Genetic distribution of 295 Bacillus cereus group members based on adk-screening in combination with MLST (Multilocus Sequence Typing) used for validating a primer targeting a chromosomal locus in B. anthracis

Journal of Microbiological Methods

Volumn 71, Issue 3, 2007, Pages 265-274

  Olsen, Jaran S ^a   Skogan, Gunnar ^a   Fykse, Else Marie ^a   Rawlinson, Elizabeth L ^a   Tomaso, Herbert ^c   Granum, Per Einar ^b   Blatny, Janet M ^a  

^a NORWEGIAN DEFENCE RESEARCH ESTABLISHMENT FFI   (Norway)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^c German Armed Forces   (Germany)

Author keywords

Bacillus cereus group; Chromosomal markers; MLST; Real time PCR

Indexed keywords

ARTICLE; BACILLUS ANTHRACIS; BACILLUS CEREUS; CHROMOSOME ANALYSIS; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADENYLATE KINASE; BACILLUS ANTHRACIS; BACILLUS CEREUS; BACTERIAL TYPING TECHNIQUES; CHROMOSOMES, BACTERIAL; DNA PRIMERS; DNA, BACTERIAL; GENETIC MARKERS; POLYMERASE CHAIN REACTION;

BACILLUS ANTHRACIS; BACILLUS CEREUS GROUP;

EID: 36348967243     PISSN: 01677012     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mimet.2007.10.001     Document Type: Article

References (56)

1. Agaisse H., Gominet M., Okstad O.A., Kolsto A.B., and Lereclus D. PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis. Mol. Microbiol. 32 (1999) 1043-1053
2. Anderson Borge G.I., Skeie M., Sorhaug T., Langsrud T., and Granum P.E. Growth and toxin profiles of Bacillus cereus isolated from different food sources. Int. J. Food Microbiol. 69 (2001) 237-246
3. Bode E., Hurtle W., and Norwood D. Real-time PCR assay for a unique chromosomal sequence of Bacillus anthracis. J. Clin. Microbiol. 42 (2004) 5825-5831
4. Cherif A., Borin S., Rizzi A., Ouzari H., Boudabous A., and Daffonchio D. Bacillus anthracis diverges from related clades of the Bacillus cereus group in 16S-23S ribosomal DNA intergenic transcribed spacers containing tRNA genes. Appl. Environ. Microbiol. 69 (2003) 33-40
5. Cherif A., Brusetti L., Borin S., Rizzi A., Boudabous A., Khyami-Horani H., and Daffonchio D. Genetic relationship in the 'Bacillus cereus group' by rep-PCR fingerprinting and sequencing of a Bacillus anthracis-specific rep-PCR fragment. J. Appl. Microbiol. 94 (2003) 1108-1119
6. Daffonchio D., Raddadi N., Merabishvili M., Cherif A., Carmagnola L., Brusetti L., Rizzi A., Chanishvili N., Visca P., Sharp R., and Borin S. Strategy for identification of Bacillus cereus and Bacillus thuringiensis strains closely related to Bacillus anthracis. Appl. Environ. Microbiol. 72 (2006) 1295-1301
7. de Maagd R.A., Bravo A., and Crickmore N. How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet 17 (2001) 193-199
8. Di Franco C., Beccari E., Santini T., Pisaneschi G., and Tecce G. Colony shape as a genetic trait in the pattern-forming Bacillus mycoides. BMC Microbiol. 13 (2002) 33 Electronic publication
9. Drobniewski F.A. Bacillus cereus and related species. Clin. Microbiol. Rev. 6 (1993) 324-338
10. Dwyer K.G., Lamonica J.M., Schumacher J.A., Williams L.E., Bishara J., Lewandowski A., Redkar R., Patra G., and DelVecchio V.G. Identification of Bacillus anthracis specific chromosomal sequences by suppressive subtractive hybridization. BMC Genomics 5 (2004) 15
11. Easterday W.R., Van Ert M.N., Simonson T.S., Wagner D.M., Kenefic L.J., Allender C.J., and Keim P. Use of single nucleotide polymorphisms in the plcr gene for specific identification of Bacillus anthracis. J. Clin. Microbiol. 43 (2005) 1995-1997
12. Ellerbrok H., Nattermann H., Ozel M., Beutin L., Appel B., and Pauli G. Rapid and sensitive identification of pathogenic and apathogenic Bacillus anthracis by real-time PCR. FEMS Microbiol. Lett. 214 (2002) 51-59
13. Farrar W.E., and Reboli A.C. The genus Bacillus-medical. In: Balows A., Trüper H.G., Dworkin M., Harder W., and Schleifer K.H. (Eds). The Prokaryotes: a handbook on the biology of bacteria: ecophysiology, isolation, identification, applications (1992), Springer-Verlag, New York 1758-1759
14. Granum P.E. Bacillus cereus. In: Doyle M.P., and Beuchat L.R. (Eds). Food Microbiology. Fundamentals and Frontiers. 3. edition (2007), ASM Press, Washington DC 445-455
15. Han C.S., Xie G., Challacombe J.F., Altherr M.R., Bhotika S.S., Brown N., Bruce D., Campbell C.S., Campbell M.L., Chen J., Chertkov O., Cleland C., Dimitrijevic M., Doggett N.A., Fawcett J.J., Glavina T., Goodwin L.A., Green L.D., Hill K.K., Hitchcock P., Jackson P.J., Keim P., Kewalramani A.R., Longmire J., Lucas S., Malfatti S., McMurry K., Meincke L.J., Misra M., Moseman B.L., Mundt M., Munk A.C., Okinaka R.T., Parson-Quintana B., Reilly L.P., Richardson P., Robinson D.L., Rubin E., Saunders E., Tapia R., Tesmer J.G., Thayer N., Thompson L.S., Tice H., Ticknor L.O., Wills P.L., Brettin T.S., and Gilna P. Pathogenomic sequence analysis of Bacillus cereus and Bacillus thuringiensis isolates closely related to Bacillus anthracis. J. Bacteriol. 188 (2006) 3382-3390
16. Harrell L.J., Andersen G.L., and Wilson K.H. Genetic variability of Bacillus anthracis and related species. J. Clin. Microbiol. 33 (1995) 1847-1850
17. Helgason E., Caugant D.A., Lecadet M.M., Chen Y., Mahillon J., Lovgren A., Hegna I., Kvaloy K., and Kolsto A.B. Genetic diversity of Bacillus cereus/B. thuringiensis isolates from natural sources. Curr. Microbiol. 37 (1998) 80-87
18. Helgason E., Okstad O.A., Caugant D.A., Johansen H.A., Fouet A., Mock M., Hegna I., and Kolsto A.B. Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis-one species on the basis of genetic evidence. Appl. Environ. Microbiol. 66 (2000) 2627-2630
19. Helgason E., Tourasse N.J., Meisal R., Caugant D.A., and Kolsto A.B. Multilocus sequence typing scheme for bacteria of the Bacillus cereus group. Appl. Environ. Microbiol. 70 (2004) 191-201
20. Hill K.K., Ticknor L.O., Okinaka R.T., Asay M., Blair H., Bliss K.A., Laker M., Pardington P.E., Richardson A.P., Tonks M., Beecher D.J., Kemp J.D., Kolsto A.B., Wong A.C., Keim P., and Jackson P.J. Fluorescent amplified fragment length polymorphism analysis of Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis isolates. Appl. Environ. Microbiol. 70 (2004) 1068-1080
21. Hoffmaster A.R., Meyer R.F., Bowen M.D., Marston C.K., Weyant R.S., Thurman K., Messenger S.L., Minor E.E., Winchell J.M., Rassmussen M.V., Newton B.R., Parker J.T., Morrill W.E., McKinney N., Barnett G.A., Sejvar J.J., Jernigan J.A., Perkins B.A., and Popovic T. Evaluation and validation of a real-time polymerase chain reaction assay for rapid identification of Bacillus anthracis. Emerg. Infect. Dis. 8 (2002) 1178-1182
22. Hoffmaster A.R., Ravel J., Rasko D.A., Chapman G.D., Chute M.D., Marston C.K., De B.K., Sacchi C.T., Fitzgerald C., Mayer L.W., Maiden M.C., Priest F.G., Barker M., Jiang L., Cer R.Z., Rilstone J., Peterson S.N., Weyant R.S., Galloway D.R., Read T.D., Popovic T., and Fraser C.M. Identification of anthrax toxin genes in a Bacillus cereus associated with an illness resembling inhalation anthrax. Proc. Natl. Acad. Sci. 101 (2004) 8449-8454
23. Hoffmaster A.R., Hill K.K., Gee J.E., Marston C.K., De B.K., Popovic T., Sue D., Wilkins P.P., Avashia S.B., Drumgoole R., Helma C.H., Ticknor L.O., Okinaka R.T., and Jackson P.J. 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 (2006) 3352-3360
24. Hurtle W., Bode E., Kulesh D.A., Kaplan R.S., Garrison J., Bridge D., House M., Frye M.S., Loveless B., and Norwood D. Detection of the Bacillus anthracis gyrA gene by using a minor groove binder probe. J. Clin. Microbiol. 42 (2004) 179-185
25. Inglesby T.V., O'Toole T., Henderson D.A., Bartlett J.G., Ascher M.S., Eitzen E., Friedlander A.M., Gerberding J., Hauer J., Hughes J., McDade J., Osterholm M.T., Parker G., Perl T.M., Russell P.K., Tonat K., and Working Group on Civilian Biodefense. Anthrax as a biological weapon, 2002: updated recommendations for management. JAMA 287 (2002) 2236-2252
26. Jacobsson S., Issa M., Unemo M., Backman A., Molling P., Sulaiman N., and Olcen P. Molecular characterisation of group A Neisseria meningitidis isolated in Sudan 1985-2001. APMIS 111 (2003) 1060-1066
27. Keim P., Kalif A., Schupp J., Hill K., Travis S.E., Richmond K., Adair D.M., Hugh-Jones M., Kuske C.R., and Jackson P. Molecular evolution and diversity in Bacillus anthracis as detected by amplified fragment length polymorphism markers. J. Bacteriol. 179 (1997) 818-824
28. Keim P., Price L.B., Klevytska A.M., Smith K.L., Schupp J.M., Okinaka R., Jackson P.J., and Hugh-Jones M.E. Multiple-locus variable-number tandem repeat analysis reveals genetic relationships within Bacillus anthracis. J. Bacteriol. 182 (2000) 2928-2936
29. Kim K., Seo J., Wheeler K., Park C., Kim D., Park S., Kim W., Chung S.I., and Leighton T. Rapid genotypic detection of Bacillus anthracis and the Bacillus cereus group by multiplex real-time PCR melting curve analysis. FEMS Immunol. Med. Microbiol. 43 (2005) 301-310
30. Ko K.S., Kim J.W., Kim J.M., Kim W., Chung S.I., Kim I.J., and Kook Y.H. Population structure of the Bacillus cereus group as determined by sequence analysis of six housekeeping genes and the plcR gene. Infect. Immun. 72 (2004) 5253-5261
31. Kotetishvili M., Stine O.C., Chen Y., Kreger A., Sulakvelidze A., Sozhamannan S., and Morris Jr. J.G. Multilocus sequence typing has better discriminatory ability for typing Vibrio cholerae than does pulsed-field gel electrophoresis and provides a measure of phylogenetic relatedness. J. Clin. Microbiol. 41 (2003) 2191-2196
32. Kotetishvili M., Kreger A., Wauters G., Morris Jr. J.G., Sulakvelidze A., and Stine O.C. Multilocus sequence typing for studying genetic relationships among Yersinia species. J. Clin. Microbiol. 43 (2005) 2674-2684
33. Kumar S., Tamura K., and Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5 (2004) 150-163
34. Maiden M.C., Bygraves J.A., Feil E., Morelli G., Russell J.E., Urwin R., Zhang Q., Zhou J., Zurth K., Caugant D.A., Feavers I.M., Achtman M., and Spratt B.G. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. 95 (1998) 3140-3145
35. Manning G., Dowson C.G., Bagnall M.C., Ahmed I.H., West M., and Newell D.G. Multilocus sequence typing for comparison of veterinary and human isolates of Campylobacter jejuni. Appl. Environ. Microbiol. 69 (2003) 6370-6379
36. Marston C.K., Gee J.E., Popovic T., and Hoffmaster A.R. Molecular approaches to identify and differentiate Bacillus anthracis from phenotypically similar Bacillus species isolates. BMC Microbiol. 3 (2006) 22
37. Nakamura L.K. Bacillus pseudomycoides sp. Int. J. Syst. Bacteriol. 48 (1998) 1031-1035
38. Patra G., Sylvestre P., Ramisse V., Therasse J., and Guesdon J.L. Isolation of a specific chromosomic DNA sequence of Bacillus anthracis and its possible use in diagnosis. FEMS Immunol. Med. Microbiol. 15 (1996) 223-231
39. Pearson T., Busch J.D., Ravel J., Read T.D., Rhoton S.D., U'Ren J.M., Simonson T.S., Kachur S.M., Leadem R.R., Cardon M.L., Van Ert M.N., Huynh L.Y., Fraser C.M., and Keim P. Phylogenetic discovery bias in Bacillus anthracis using single-nucleotide polymorphisms from whole-genome sequencing. Proc. Natl. Acad. Sci. 14 (2004) 13536-13541
40. Pillai A., Thomas S., and Arora J. Bacillus cereus: the forgotten pathogen. Surg. Infect. Larchmt. 7 (2006) 305-308
41. Priest F.G., Barker M., Baillie L.W., Holmes E.C., and Maiden M.C. Population structure and evolution of the Bacillus cereus group. J. Bacteriol. 186 (2004) 7959-7970
42. Qi Y., Patra G., Liang X., Williams L.E., Rose S., Redkar R.J., and DelVecchio V.G. Utilization of the rpoB gene as a specific chromosomal marker for real-time PCR detection of Bacillus anthracis. Appl. Environ. Microbiol. 67 (2001) 3720-3727
43. Radnedge L., Agron P.G., Hill K.K., Jackson P.J., Ticknor L.O., Keim P., and Andersen G.L. Genome differences that distinguish Bacillus anthracis from Bacillus cereus and Bacillus thuringiensis. Appl. Environ. Microbiol. 69 (2003) 2755-2764
44. Ramisse V., Patra G., Garrigue H., Guesdon J.L., and Mock M. Identification and characterization of Bacillus anthracis by multiplex PCR analysis of sequences on plasmids pXO1 and pXO2 and chromosomal DNA. FEMS Microbiol. Lett. 145 (1996) 9-16
45. Ramisse V., Patra G., Vaissaire J., and Mock M. The Ba813 chromosomal DNA sequence effectively traces the whole Bacillus anthracis community. J. Appl. Microbiol. 87 (1999) 224-228
46. Rasko D.A., Altherr M.R., Han C.S., and Ravel J. Genomics of the Bacillus cereus group of organisms. FEMS Microbiol. Rev. 29 (2005) 303-329
47. Saitou N., and Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 (1987) 406-425
48. Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., Zeigler D.R., and Dean D.H. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62 (1998) 775-806
49. Schoeni J.L., and Wong A.C. Bacillus cereus food poisoning and its toxins. Review. J. Food. Prot. 68 (2005) 636-648
50. Staden R. The Staden sequence analysis package. Mol. Biotechnol. 5 (1996) 233-241
51. Stenfors L.P., Mayr R., Scherer S., and Granum P.E. Pathogenic potential of fifty Bacillus weihenstephanensis strains. FEMS Microbiol. Lett., 215 (2002) 47-51
52. Tartofm S.Y., Solberg O.D., Manges A.R., and Riley L.W. Analysis of a uropathogenic Escherichia coli clonal group by multilocus sequence typing. J. Clin. Microbiol. 43 (2005) 5860-5864
53. Turnbull P.C., Hutson R.A., Ward M.J., Jones M.N., Quinn C.P., Finnie N.J., Duggleby C.J., Kramer J.M., and Melling J. Bacillus anthracis but not always anthrax. J. Appl. Bacteriol. 72 (1992) 21-28
54. Valjevac S., Hilaire V., Lisanti O., Ramisse F., Hernandez E., Cavallo J.D., Pourcel C., and Vergnaud G. Comparison of minisatellite polymorphisms in the Bacillus cereus complex: a simple assay for large-scale screening and identification of strains most closely related to Bacillus anthracis. Appl. Environ. Microbiol. 71 (2005) 6613-6623
55. Van Ert M.N., Easterday W.R., Huynh L.Y., Okinaka R.T., Hugh-Jones M.E., Ravel J., Zanecki S.R., Pearson T., Simonson T.S., U'Ren J.M., Kachur S.M., Leadem-Dougherty R.R., Rhoton S.D., Zinser G., Farlow J., Coker P.R., Smith K.L., Wang B., Kenefic L.J., Fraser-Liggett C.M., Wagner D.M., and Keim P. Global genetic population structure of Bacillus anthracis. PLoS ONE 23 2 (2007) e461
56. Vassileva M., Torii K., Oshimoto M., Okamoto A., Agata N., Yamada K., Hasegawa T., and Ohta M. Phylogenetic analysis of Bacillus cereus isolates from severe systemic infections using multilocus sequence typing scheme. Microbiol. Immunol 50 (2006) 743-749