Abstract
Bacillus cereus sensu lato group, which includes the causative agent of anthrax Bacillus anthracis, has a high degree of genetic similarity. However, in recent years, the development of molecular genetics has made it possible to find some molecular markers for identifying Bacillus anthracis in order to differentiate it from the closely related bacilli, get the clustering of the collection of strains, and describe the phylogenetic relationships between the clusters. This article deals with up-to-date methods of genotyping of Bacillus anthracis; it also evaluates its discrimination ability, informational value, validity of the results, efficiency, simplicity, and ease of use. In addition, international online resources and the possibility of their use for comparing collections of the B. anthracis strains isolated from various parts of the world are discussed.
Similar content being viewed by others
References
Léonard, C., Chen, Y., and Mahillon, J., Diversity and differential distribution of IS231, IS232 and IS240 among Bacillus cereus, Bacillus thuringiensis and Bacillus mycoides, Microbiology, 1997, vol. 143, no. 8, pp. 2537–2547. doi 10.1099/00221287-143-8-2537
Zwick, M.E., Joseph, S.J., Didelot, X., et al., Genomic characterization of the Bacillus cereus sensu lato species: backdrop to the evolution of Bacillus anthracis, Genome Res., 2012, vol. 22, no. 8, pp. 1512–1524. doi 10.1101/gr.134437.111
Keim, P., Gruendike, J.M., Klevytska, A.M., et al., The genome and variation of Bacillus anthracis, Mol. Aspects Med., 2009, vol. 30, pp. 397–405. doi 10.1016/j.mam.2009.08.005
Keim, P., Price, L.B., Klevytska, A.M., et al., Multiple-locus variable-number tandem repeat analysis reveals genetic relationships within Bacillus anthracis, J. Bacteriol., 2000, vol. 182, pp. 2928–2936. doi 0.1128/jb.182.10.2928-2936.2000
Pearson, T., Busch, J.D., Ravel, J., et al., Phylogenetic discovery bias in Bacillus anthracis using single-nucleotide polymorphisms from whole-genome sequencing., Proc. Natl. Acad. Sci. U.S.A., 2004, vol. 101, pp. 13536–13541. doi 10.1073/pnas.0403844101
Achtman, M., Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens, Annu. Rev. Microbiol., 2008, vol. 62, pp. 53–70. pmid:18785837 doi 10.1146/annurev.micro. 62.081307.162832
Blouin, Y., Cazajous, G., Dehan, C., et al., Progenitor “Mycobacterium canettii” clone responsible for lymph node tuberculosis epidemic Djibouti, Emerg. Infect. Dis., 2014, vol. 20, no. 1, pp. 21–28. doi 10.3201/eid2001
Cui, Y., Yu, C., Yan, Y., et al., Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis, Proc. Natl. Acad. Sci. U.S.A., 2013, vol. 110, no. 2, pp. 577–582. 1205750110 doi 10.1073/pnas.1205750110
Van Ert, M.N., Easterday, W.R., Huynh, L.Y., et al., Global genetic population structure of Bacillus anthracis, PLoS One, 2007, vol. 2, e461. doi 10.1371/journal.pone.0000461
Kenefic, L.J., Pearson, T., Okinaka, R.T., et al., Pre-Columbian origins for North American anthrax, PLoS One, 2009, vol. 4, e4813. doi 10.1371/journal. pone.0004813
Le Flèche, P., Hauck, Y., Onteniente, L., et al., A tandem repeats database for bacterial genomes: application to the genotyping of Yersinia pestis and Bacillus anthracis, BMC Microbiol., 2001, vol. 1, p. 2. doi 10.1186/1471-2180-1-2
Lista, F., Faggioni, G., Valjevac, S., et al., Genotyping of Bacillus anthracis strains based on automated capillary 25-loci multiple locus variable-number tandem repeats analysis, BMC Microbiol., 2006, vol. 6, p. 33. doi 10.1186/1471-2180-6-33
Okutani, A., Sekizuka, T., Boldbaatar, B., et al., Phylogenetic typing of Bacillus anthracis isolated in Japan by multiple locus variable-number tandem repeats and the comprehensive single nucleotide polymorphism, J. Vet. Med. Sci., 2010, vol. 72, pp. 93–97. doi 10.1292/jvms.09-0213
Pilo, P., Perreten, V., and Frey, J., Molecular epidemiology of Bacillus anthracis: determining the correct origin, Appl. Environ. Microbiol., 2008, vol. 74, pp. 2928–2931. doi 10.1128/aem.02574-07
Stratilo, C.W., Lewis, C.T., Bryden, L., et al., Singlenucleotide repeat analysis for subtyping Bacillus anthracis isolates, J. Clin. Microbiol., 2006, vol. 44, pp. 777–782. doi 10.1128/jcm.44.3.777-782.2006
Keim, P., Van Ert, M.N., Pearson, T., et al., Anthrax molecular epidemiology and forensics: using the appropriate marker for different evolutionary scales, Infect. Genet. Evol., 2004, vol. 4, pp. 205–213. doi 10.1016/j.meegid.2004.02.005
Birdsell, D.N., Pearson, T., Price, E.P., et al., Melt analysis of mismatch amplification mutation assays Melt-MAMA: a functional study of a cost-effective SNP genotyping assay in bacterial models, PLoS One, 2012, vol. 7, p. e32866. doi 10.1371/journal.pone.0032866
Thierry, S., Tourterel, C., Le Flèche, P., et al., Genotyping of French Bacillus anthracis strains based on 31-loci multi locus VNTR analysis: epidemiology, marker evaluation, and update of the internet genotype database, PLoS One, 2014, vol. 9, no. 6. doi 10.1371/journal. pone.0095131
Fouet, A., Smith, K.L., Keys, C., et al., Diversity among French Bacillus anthracis isolates, J. Clin. Microbiol., 2002, vol. 40, pp. 4732–4734. doi 10.1128/jcm.40.12.4732-4734.2002
Patra, G., Vaissaire, J., Weber-Levy, M., et al., Molecular characterization of Bacillus strains involved in outbreaks of anthrax in France in 1997, J. Clin. Microbiol., 1998, vol. 36, pp. 3412–3414.
Gierczynski, R., Kaluzewski, S., Rakin, A., et al., Intriguing diversity of Bacillus anthracis in eastern Poland—the molecular echoes of the past outbreaks, FEMS Microbiol. Lett., 2004, vol. 239, pp. 235–240. doi 10.1016/j.femsle.2004.08.038
Fasanella, A., Van Ert, M., Altamura, S.A., et al., Molecular diversity of Bacillus anthracis in Italy, J. Clin. Microbiol., 2005, vol. 43, pp. 3398–3401. doi 10.1128/jcm.43.7.3398-3401.2005
Maho, A., Rossano, A., Hachler, H., et al., Antibiotic susceptibility and molecular diversity of Bacillus anthracis strains in Chad: detection of a new phylogenetic subgroup, J. Clin. Microbiol., 2006, vol. 44, pp. 3422–3425. doi 10.1128/jcm.01269-06
Smith, K.L., DeVos, V., Bryden, H., et al., Bacillus anthracis diversity in Kruger National Park, J. Clin. Microbiol., 2000, vol. 38, pp. 3780–3784.
Durmaz, R., Doganay, M., Sahin, M., et al., Molecular epidemiology of the Bacillus anthracis isolates collected throughout Turkey from 1983 to 2011, Eur. J. Clin. Microbiol. Infect. Dis., 2012, vol. 31, pp. 2783–2790. doi 10.1007/s10096-012-1628-4
Merabishvili, M., Natidze, M., Rigvava, S., et al., Diversity of Bacillus anthracis strains in Georgia and of vaccine strains from the former Soviet Union, Appl. Environ. Microbiol., 2006, vol. 72, pp. 5631–5636. doi 10.1128/aem.00440-06
Stratilo, C.W. and Bader, D.E., Genetic diversity among Bacillus anthracis soil isolates at fine geographic scales, Appl. Environ. Microbiol., 2012, vol. 78, pp. 6433–6437. doi 10.1128/aem.01036-12
Antwerpen, M., Ilin, D., Georgieva, E., et al., MLVA and SNP analysis identified a unique genetic cluster in Bulgarian Bacillus anthracis strains, Eur. J. Clin. Microbiol. Infect. Dis., 2011, vol. 30, pp. 923–930. doi 10.1007/s10096-011-1177-2
Eremenko, E.I., Ryazanova, A.G., Tsygankova, O.I., et al., Genotype diversity of Bacillus anthracis strains isolated from the Caucasus region, Mol. Genet. Microbiol. Virol., 2012, vol. 27, no. 2, pp. 74–78. https://doi.org/10.3103/S0891416812020024.
Beyer, W., Bellan, S., Eberle, G., et al., Distribution and molecular evolution of Bacillus anthracis genotypes in Namibia, PLoS Negl. Trop. Dis., 2012, vol. 6, e1534. doi 10.1371/journal.pntd.0001534
Hoffmaster, A.R., Fitzgerald, C.C., Ribot, E., et al., Molecular subtyping of Bacillus anthracis and the 2001 bioterrorism-associated anthrax outbreak, United States, Emerg. Infect. Dis., 2002, vol. 8, pp. 1111–1116. doi 10.3201/eid0810.020394
Cheung, D.T., Kam, K.M., Hau, K.L., et al., Characterization of a Bacillus anthracis isolate causing a rare case of fatal anthrax in a 2-year-old boy from Hong Kong, J. Clin. Microbiol., 2005, vol. 43, pp. 1992–1994. doi 10.1128/jcm.43.4.1992-1994.2005
Ryu, C., Lee, K., Hawng, H.J., et al., Molecular characterization of Korean Bacillus anthracis isolates by amplified fragment length polymorphism analysis and multilocus variable-number tandem repeat analysis, Appl. Environ. Microbiol., 2005, vol. 71, pp. 4664–4671. doi 10.1128/aem.71.8.4664-4671.2005
Ryazanova, A.G., Eremenko, E.I., Tsygankova, O.I., et al., The use of methods of the Bacillus anthracis molecular typing in the reference center for monitoring the causative agent of anthrax, Probl. Osobo Opasnykh Infekts., 2011, no. 110, pp. 68–71.
Li, S., Ma, Q., Chen, H., et al., Genetic characterization of Bacillus anthracis in Guizhou Province, Southwest of China, BMC Microbiol., 2015, vol. 15, p. 77. doi 10.1186/s12866-015-0414-8
Eremenko, E.I., Ryazanova, A.G., Tsygankova, O.I., et al., Genotypic features of Bacillus anthracis strains with different manifestations of traits associated with pathogenicity, Probl. Osobo Opasnykh Infekts., 2010, no. 2(104), pp. 53–56.
Blackburn, J.K., Odugbo, M.O., Van Ert, M., et al., Bacillus anthracis diversity and geographic potential across Nigeria, Cameroon and Chad: further support of a novel West African lineage, PLoS Negl. Trop. Dis., 2015, vol. 9, no. 8, e0003931. doi 10.1371/journal. pntd.0003931
Leski, T.A., Caswell, C.C., Pawlowski, M., et al., Identification and classification of bcl genes and proteins of Bacillus cereus group organisms and their application in Bacillus anthracis detection and fingerprinting, Appl. Environ. Microbiol., 2009, vol. 75, pp. 7163–7172. doi 10.1128/aem.01069-09
Afanas’ev, M.V., Kravets, E.V., Dugarzhapova, Z.F., et al., Comparative multilocus VNTR and SNP analysis of Bacillus anthracis vaccine strains, Mol. Genet. Microbiol. Virol., 2014, vol. 29, no. 2, pp. 86–92. https://doi.org/10.3103/S0891416814020025.
Newton, C.R., Graham, A., Heptinstall, L.E., et al., Analysis of any point mutation in DNA: the amplification refractory mutation system ARMS, Nucleic Acids. Res., 1989, vol. 17, pp. 2503–2516.
Wu, D.Y., Ugozzoli, L., Pal, B.K., and Wallace, R.B., Allele-specific enzymatic amplification of beta-globin genomic DNA for diagnosis of sickle cell anemia, Proc. Natl. Acad. Sci. U.S.A., 1989, vol. 86, pp. 2757–2760.
Papp, A.C., Pinsonneault, J.K., Cooke, G., and Sadee, W., Single nucleotide polymorphism genotyping using allele-specific PCR and fluorescence melting curves, Biotechniques, 2003, vol. 34, pp. 1068–1072.
Dall’Ozzo, S., Andres, C., Bardos, P., et al., Rapid single-step FCGR3A genotyping based on SYBR Green I fluorescence in real-time multiplex allele-specific PCR, J. Immunol. Methods, 2003, vol. 277, pp. 185–192. doi 10.1016/S0022-1759(03)00123-6
Waterfall, C.M. and Cobb, B.D., SNP genotyping using single-tube fluorescent bidirectional PCR, Biotechniques, 2002, vol. 33, no. 80, pp. 82–90.
Dobrin, S., David, D., Fieweger, K., et al., High throughput SNP genotyping using Array Tape™ in place of microplates, Plant Breed. Biotech., 2014, vol. 2, no. 3, pp. 195–212. doi 10.9787/PBB.2014.2.3.195
Chang, C.H., Chang, Y.C., and Underwood, A., VNTRDB: a bacterial variable number tandem repeat locus database, Nucleic Acids Res., 2007, vol. 35, pp. D416–D421.
Vergnaud, G., Girault, G., Thierry, S., et al., Comparison of French and worldwide Bacillus anthracis strains favors a recent, post-Columbian origin of the predominant North-American clade, PLoS One, 2016, vol. 10, no. 8, e0135346. doi 10.1371/journal.pone.0146216
Maiden, M.C., Bygraves, J.A., Feil, E., et al., Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms, Proc. Natl. Acad. Sci. U.S.A., 1998, vol. 95, pp. 3140–3145. http://www.pnas.org/content/95/6/3140.full.pdf.
Jacobsson, S., Issa, M., Unemo, M., et al., Molecular characterisation of group A Neisseria meningitidis isolated in Sudan 1985—2001, APMIS, 2003, vol. 111, pp. 1060–1066. doi 10.1128/JCM.44.3.861-871.2006
Kotetishvili, M., Stine, O.C., Chen, Y., et al., Multilocus sequence typing has better discriminatory ability for typing Vibrio cholerae than does pulsed field gel electrophoresis and provides a measure of phylogenetic relatedness, Clin. Microbiol., 2003, vol. 41, pp. 2191–2196. doi 10.1128/JCM.41.5.2191-2196.2003
Kotetishvili, M., Kreger, A., Wauters, G., et al., Multilocus sequence typing for studying genetic relationships among Yersinia species, J. Clin. Microbiol., 2005, vol. 43, pp. 2674–2684. doi 10.1128/JCM.43.6.2674-2684.2005
Manning, G., Dowson, C.G., Bagnall, M.C., et al., Multilocus sequence typing for comparison of veterinary and human isolates of Campylobacter jejuni, Appl. Environ. Microbiol., 2003, vol. 69, pp. 6370–6379. doi 10.1128/AEM.69.11.6370-6379.2003
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., 2005, vol. 43, pp. 5860–5864. doi 10.1128/JCM.43.12.5860-5864.2005
Daffonchio, D., Raddadi, N., Merabishvili, M., et al., Strategy for identification of Bacillus cereus and Bacillus thuringiensis strains closely related to Bacillus anthracis, Appl. Environ. Microbiol., 2006, vol. 72, pp. 1295–1301. doi 10.1128/AEM.72.2.1295-1301.2006
Helgason, E., Tourasse, Ni.J., Meisal, R., et al., Multilocus sequence typing scheme for bacteria of the Bacillus cereus group, Appl. Environ. Microbiol., 2004, vol. 70, no. 1, pp. 191–201. doi 10.1128/AEM.70.1.191-201.2004
Ko, K.S., Kim, J.W., Kim, J.M., et al., Population structure of the Bacillus cereus group as determined by sequence analysis of six housekeeping genes and the plcR gene, Infect. Immun., 2004, vol. 72, pp. 5253–5261. doi 10.1128/IAI.72.9.5253-5261.2004
Priest, F.G., Barker, M., Baillie, L.W., et al., Population structure and evolution of the Bacillus cereus group, J. Bacteriol., 2004, vol. 186, no. 23, pp. 7959–7970. doi 10.1128/JB.186.23.7959-7970.2004
Agaisse, H., Gominet, M., Okstad, O.A., et al., PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis, Mol. Microbiol., 1999, vol. 32, pp. 1043–1053. doi 10.1046/j.1365-2958.1999.01419.x
Cardazzo, B., Negrisolo, E., Carraro, L., et al., Multiplelocus sequence typing and analysis of toxin genes in Bacillus cereus Food-Borne Isolates, Appl. Environ. Microbiol., 2008, vol. 74, no. 3, pp. 850–860. doi 10.1128/AEM.01495-07
Larsson, P., Svensson, K., Karlsson, L., et al., Canonical insertion-deletion markers for rapid DNA typing of Francisella tularensis, Emerg. Infect. Dis., 2007, vol. 13, no. 11, pp. 1725–1732. doi 10.3201/eid1311.070603
Read, T.D., Salzberg, S.L., Pop, M., et al., Comparative genome sequencing for discovery of novel polymorphisms in Bacillus anthracis, Science, 2002, vol. 296, pp. 2028–2033. doi 10.1126/science.1071837
Ahmod, N.Z., Gupta, R.S., and Shah, H.N., development of a rapid pyrosequencing assay for distinguishing B. anthracis from the B. cereus group, J. Microbiol. Methods, 2011, vol. 87, no. 3, pp. 278–285. doi 10.1016/j.mimet.2011.08.015
Mokrievich, A.N., Kudryavtseva, T.Yu., Varlamov, D.A., Sochivko, D.G., and Dyatlov, I.A., Patent RU 0002542395 C1, Byull. Izobret. Polezn. Modeli, 2015, no. 5. http://www1.fips.ru/wps/wcm/connect/content_ru/ru/ofic_publofic_bul/ofic_bul_izpo/.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © V.S. Timofeev, I.V. Bakhteeva, I.A. Dyatlov, 2018, published in Genetika, 2018, Vol. 54, No. 1, pp. 3–14.
Rights and permissions
About this article
Cite this article
Timofeev, V.S., Bakhteeva, I.V. & Dyatlov, I.A. Genotyping of Bacillus anthracis and Closely Related Microorganisms. Russ J Genet 54, 1–11 (2018). https://doi.org/10.1134/S1022795418010118
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1022795418010118