Identification of a Bacillus anthracis specific indel in the yeaC gene and development of a rapid pyrosequencing assay for distinguishing B. anthracis from the B. cereus group

Journal of Microbiological Methods

Volumn 87, Issue 3, 2011, Pages 278-285

  Ahmod, Nadia Z ^a   Gupta, Radhey S ^b   Shah, Haroun N ^a  

^a PUBLIC HEALTH ENGLAND   (United Kingdom)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Anthracis specific indel; B. anthracis; B. cereus; Pyrosequencing; Rapid detection; YeaC protein

Indexed keywords

BACTERIAL PROTEIN; UNCLASSIFIED DRUG; YEAC PROTEIN;

AGAR GEL ELECTROPHORESIS; ARTICLE; BACILLUS ANTHRACIS; BACILLUS CEREUS; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL MUTATION; BACTERIAL VIRULENCE; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; CHROMOSOME MARKER; CONTROLLED STUDY; GENE EXPRESSION REGULATION; INDEL MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROTEIN EXPRESSION; PYROSEQUENCING; SPECIES DIFFERENCE; YEAC GENE;

ANIMALS; BACILLUS ANTHRACIS; BACILLUS CEREUS; BACTERIAL PROTEINS; BACTERIOLOGICAL TECHNIQUES; DNA PRIMERS; ELECTROPHORESIS, AGAR GEL; HUMANS; INDEL MUTATION; POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS, DNA;

BACILLUS ANTHRACIS; BACILLUS CEREUS; BACILLUS CEREUS GROUP; BACILLUS MYCOIDES; BACILLUS PSEUDOMYCOIDES; BACILLUS THURINGIENSIS;

EID: 81055155829     PISSN: 01677012     EISSN: 18728359     Source Type: Journal    
DOI: 10.1016/j.mimet.2011.08.015     Document Type: Article

References (53)

1. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
2. Ash C., Farrow J.A.E., Dorsch M., Stackebrandt E., Collins M.D. Comparative analysis of Bacillus anthracis, Bacillus cereus, and related species on the basis of reverse transcriptase sequencing of 16S rRNA. Int. J. Syst. Bacteriol. 1991, 41:343-346.
3. Barker M., Thakker B., Priest F.G. Multilocus sequence typing reveals that Bacillus cereus strains isolated from clinical infections have distinct phylogenetic origins. FEMS Microbiol. Lett. 2005, 245:179-184.
4. Bavykin S.G., Yuri L.P., Vladimir Z., Kelly J.J., Jackman J., Stahl D.A., Cherni A. Use of 16S rRNA, 23S rRNA, and gyrB gene sequence analysis to determine phylogenetic relationships of Bacillus cereus group microorganisms. J. Clin. Microbiol. 2004, 42:3711-3730.
5. Bell C.A., Uhl J.R., Hadfield T.L., David J.C., Meyer R.F., Smith T.F., Cockerill F.R. Detection of Bacillus anthracis DNA by LightCycler PCR. J. Clin. Microbiol. 2002, 40:2897-2902.
6. Blackwood K.S., Turenne C.Y., Harmsen D., Kabani A.M. Reassessment of sequence-based targets for identification of Bacillus species. J. Clin. Microbiol. 2004, 42:1626-1630.
7. Borriss R., Porwollik S., Schroeter R. The 52°-55° segment of the Bacillus subtilis chromosome: a region devoted to purine uptake and metabolism, and containing the genes cotA, gabP and guaA and the pur gene cluster within a 34960bp nucleotide sequence. Microbiology 1996, 142:3027-3031.
8. Carlson C.R., Caugant D.A., Kolstø A. Genotypic diversity among Bacillus cereus and Bacillus thuringiensis strains. Appl. Environ. Microbiol. 1994, 60:1719-1725.
9. Chen M.L., Tsen H.Y. Discrimination of Bacillus cereus and Bacillus thuringiensis with 16S rRNA and gyrB gene based PCR primers and sequencing of their annealing sites. J. Appl. Microbiol. 2002, 92:912-919.
10. Daffonchio D., Cherif A., Borin S. Homoduplex and heteroduplex polymorphisms of the amplified ribosomal 16 S-23 S internal transcribed spacers describe genetic relationships in the "Bacillus cereus group". Appl. Environ. Microbiol. 2000, 66:5460-5468.
11. Drobniewski F.A. Bacillus cereus and related species. Clin. Microbiol. Rev. 1993, 6:324-338.
12. Ellerbrok H., Nattermann H., Ozel M., Beutin L., Appel B., Pauli G. Rapid andsensitive identification of pathogenic and apathogenic Bacillus anthracis by realtime PCR. FEMS Microbiol. Lett. 2002, 214:51-59.
13. Fasanella A., Losito S., Adone R., Ciuchini F., Trotta T., Altamura S.A., Chiocco D., Ippolito G. PCR assay to detect Bacillus anthracis spores in heat-treated specimens. J. Clin. Microbiol. 2003, 41:896-899.
14. Fritze D. Taxonomy of the genus Bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathology 2004, 94:1245-1248.
15. Gao B., Gupta R.S. Conserved indels in protein sequences that are characteristic of the phylum Actinobacteria. Int. J. Syst. Evol. Microbiol. 2005, 55:2401-2412.
16. Gao B., Mohan R., Gupta R.S. Phylogenomics and protein signatures elucidating the evolutionary relationships among the Gammaproteobacteria. Int. J. Syst. Evol. Microbiol. 2009, 59:234-247.
17. Griffiths E., Petrich A.K., Gupta R.S. Conserved indels in essential proteins that are distinctive characteristics of Chlamydiales and provide novel means for their identification. Microbiology 2005, 151:2647-2657.
18. Gupta R.S. Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades. Int. J. Syst. Evol. Microbiol. 2009, 59:2510-2526.
19. Gupta R.S., Gao B. Phylogenomic analyses of clostridia and identification of novel protein signatures that are specific to the genus Clostridium sensu stricto (cluster I). Int. J. Syst. Evol. Microbiol. 2009, 59:285-294.
20. Gupta R.S., Griffiths E. Critical issues in bacterial phylogeny. Theor. Popul. Biol. 2002, 61:423-434.
21. Gupta R.S., Griffiths E. Chlamydiae-specific proteins and indels: novel tools for studies. Trends Microbiol. 2006, 14:527-535.
22. Gupta R.S., Lorenzini E. Phylogeny and molecular signatures (conserved proteins and indels) that are specific for the Bacteroidetes and Chlorobi species. BMC Evol. Microbiol. 2007, 7:71-89.
23. Gupta R.S., Mok A. Phylogenomics and signature proteins for the alpha Proteobacteria and its main groups. BMC Microbiol. 2007, 7:106-126.
24. Hadjinicolaou A.V., Demetriou V.L., Hezka J., Beyer W., Hadfield T.L., Kostrikis L.G. Use of molecular beacons and multi-allelic real-time PCR for detection of and discrimination between virulent Bacillus anthracis and other Bacillus isolates. J. Microbiol. Methods 2009, 78:45-53.
25. Hall T.A. Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41:95-98.
26. 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., Gilna P. Pathogenomic sequence analysis of Bacillus cereus and Bacillus thuringiensis isolates closely related to Bacillus anthracis. J. Bacteriol. 2006, 188:3382-3390.
27. Hansen B.M., Hendriksen N.B. Detection of enterotoxic Bacillus cereus and Bacillus thuringiensis strains by PCR analysis. Appl. Environ. Microbiol. 2001, 67:185-189.
28. Helgason E., Okstad O.A., Caugant D.A., Johansen H.A., Fouet A., Mock M., Hegna I., Kolstø A.B. Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis-one species on the basis of genetic evidence. Appl. Environ. Microbiol. 2000, 66:2627-2630.
29. Helgason E., Tourasse N.J., Meisal R., Caugant D.A., Kolstø A. Multilocus sequence typing scheme for bacteria of the Bacillus cereus group. Appl. Environ. Microbiol. 2004, 70:191-201.
30. 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., 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. 2006, 44:3352-3360.
31. Hurtle W., Bode E., Kulesh D.A., Kaplan R.S., Garrison J., Bridge D., House M., Frye M.S., Loveless B., Norwood D. Detection of the Bacillus anthracis gyrA gene by using a minor groove binder probe. J. Clin. Microbiol. 2004, 42:179-185.
32. Jensen G.B., Hansen B.M., Eilenberg J., Mahillon J. The hidden lifestyles of Bacillus cereus and relatives. Environ. Microbiol. 2003, 5:631-640.
33. Klee S.R., Brzuszkiewicz E.B., Nattermann H., Brüggemann H., Dupke S., Wollherr A., Franz T., Pauli G., Appel B., Liebl W., Couacy-Hymann E., Boesch C., Meyer F., Leendertz F.H., Ellerbrok H., Gottschalk G., Grunow R., Liesegang H. The genome of a Bacillus isolate causing anthrax in chimpanzees combines chromosomal properties of B. cereus with B. anthracis virulence plasmids. PLoS One 2010, 5:e10986.
34. Ko K.S., Kim J.M., Kim J.W., Jung B.Y., Kim W., Kim I.J., Kook Y.H. Identification of Bacillus anthracis by rpoB sequence analysis and multiplex PCR. J. Clin. Microbiol. 2003, 41:2908-2914.
35. Kolstø A.B., Tourasse N.J., Okstad O.A. What sets Bacillus anthracis apart from other Bacillus species?. Annu. Rev. Microbiol. 2009, 63:451-476.
36. La Duc M.T., Satomi M., Agata N., Venkateswaran K. GyrB as a phylogenetic discriminator for the members of the Bacillus anthracis-cereus-thuringiensis group. J. Microbiol. Methods 2004, 56:383-394.
37. Lechner S., Mayr R., Francis K.P., Prüß B.M., Kaplan T., Wießner-Gunkel E., Stewart G.S.A.B., Scherer S. Bacillus weihenstephanensis sp. nov. is a new psychrotolerant species of the Bacillus cereus group. Int. J. Syst. Evol. Microbiol. 1998, 48:1373-1382.
38. Mock M., Fouet A. Anthrax. Annu. Rev. Microbiol. 2001, 55:647-671.
39. Nakamura L.K., Jackson M.A. Clarification of the taxonomy of Bacillus mycoides. Int. J. Syst. Bacteriol. 1995, 45:46-49.
40. Oggioni M.R., Meacci F., Carattoli A., Ciervo A., Orru G., Cassone A., Pozzi G. Protocol for real-time PCR identification of anthrax spores from nasal swabs after broth enrichment. J. Clin. Microbiol. 2002, 40:3956-3963.
41. 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., Ert M.N., Huynh L.Y., Fraser K.M., Keim P. Phylogenetic discovery bias in Bacillus anthracis using single-nucleotide polymorphisms from whole-genome sequencing. PNAS 2004, 101:13536-13541.
42. Priest F.G., Barker M., Baillie L.W.J., Holmes E.C., Maiden M.C.J. Population structure and evolution of the Bacillus cereus group. J. Bacteriol. 2004, 186:7959-7970.
43. Qi Y., Patra G., Liang X., Williams L.E., Rose S., Redkar R.J., Delvecchio V.G. Utilization of the rpoB gene as a specific chromosomal marker for real-time PCR detection of Bacillus anthracis. Appl. Environ. Microbiol. 2001, 67:3720-3727.
44. Ramisse V., Patra G., Vaissaire J., Mock M. The Ba813 chromosomal DNA sequence effectively traces the whole Bacillus anthracis community. J. Appl. Microbiol. 1999, 87:224-228.
45. Rao S.S., Mohan K.V., Atreya C.D. Detection technologies for Bacillus anthracis: prospects and challenges. J. Microbiol. Methods 2010, 82:1-10.
46. Read T.D., Peterson S.N., Tourasse N., Baillie L.W., Paulsen I.T., Nelson K.E., Tettelin H., Fouts D.E., Eisen J.A., Gill S.R., Holtzapple E.K., Okstad O.A., Helgason E., Rilstone J., Wu M., Kolonay J.F., Beanan M.J., Dodson R.J., Brinkac L.M., Gwinn M., DeBoy R.T., Madpu R., Daugherty S.C., Durkin A.S., Haft D.H., Nelson W.C., Peterson J.D., Pop M., Khouri H.M., Radune D., Benton J.L., Mahamoud Y., Jiang L., Hance I.R., Weidman J.F., Berry K.J., Plaut R.D., Wolf A.M., Watkins K.L., Nierman W.C., Hazen A., Cline R., Redmond C., Thwaite J.E., White O., Salzberg S.L., Thomason B., Friedlander A.M., Koehler T.M., Hanna P.C., Kolstø A.B., Fraser C.M. The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature 2003, 423:81-86.
47. Ronaghi M. Pyrosequencing sheds light on DNA sequencing. Genome Res. 2001, 11:3-11.
48. Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., Zeigler D.R., Dean D.H. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 1998, 62:775-806.
49. Slinger R., Yan L., Myers R., Ramotar K., St Denis M., Aaron S.D. Pyrosequencing of a recA gene variable region for Burkholderia cepacia complex genomovar identification. Diagn. Microbiol. Infect. Dis. 2007, 58:379-384.
50. Snider J., Houry W.A. MoxR AAA+ ATPases: A novel family of molecular chaperones?. J. Struct. Biol. 2006, 156:200-209.
51. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
52. Ticknor L.O., Kolstø A.B., Hill K., Keim P., Laker M.T., Tonks M., Jackson P.J. Fluorescent amplified fragment length polymorphism analysis of Norwegian Bacillus cereus and Bacillusithuringiensis soil isolates. Appl. Environ. Microbiol. 2001, 67:4863-4873.
53. Wahab T., Hjalmarsson S., Wollin R., Engstrand L. Pyrosequencing Bacillus anthracis. Emerg. Infect. Dis. 2005, 11.