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

Volumn 9, Issue 6, 2014, Pages

  Thierry, Simon ^a   Tourterel, Christophe ^b,c   Le Fléche, Philippe ^b,c,d   Derzelle, Sylviane ^a   Dekhil, Neira ^a   Mendy, Christiane ^a   Colaneri, Cécile ^a   Vergnaud, Gilles ^b,c,e   Madani, Nora ^a  

^a UNIVERSITÉ PARIS EST   (France)

^b INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^c CNRS   (France)

^d Delegation Generale pour l'Armement   (France)

^e DGA/MRIS Mission pour la Recherche et l'Innovation Scientifique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

31 LOCI MULTIPLE LOCUS VARIABLE NUMBER TANDEM REPEAT ANALYSIS; 7 LOCI MULTIPLE LOCUS VARIABLE NUMBER TANDEM REPEAT ANALYSIS; AGAR GEL ELECTROPHORESIS; ARTICLE; BACILLUS ANTHRACIS; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIUM EXAMINATION; CLONAL VARIATION; COMPUTER PROGRAM; COST; FRANCE; GENE CLUSTER; GENE LOCUS; GENETIC DATABASE; GENETIC MARKER; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHICAL VARIATION (SPECIES); INTERMETHOD COMPARISON; MOLECULAR EPIDEMIOLOGY; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; VARIABLE NUMBER OF TANDEM REPEAT; ANTHRAX; CLASSIFICATION; CLUSTER ANALYSIS; GENETICS; HUMAN; INTERNET; MICROBIOLOGY; NUCLEIC ACID DATABASE; TOPOGRAPHY;

GENETIC MARKER;

ANTHRAX; BACILLUS ANTHRACIS; CLUSTER ANALYSIS; DATABASES, NUCLEIC ACID; FRANCE; GENETIC MARKERS; GENOTYPE; HUMANS; INTERNET; MINISATELLITE REPEATS; MULTILOCUS SEQUENCE TYPING; POLYMORPHISM, SINGLE NUCLEOTIDE; TOPOGRAPHY, MEDICAL;

EID: 84902491289     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095131     Document Type: Article

References (47)

1. Turnbull PC (2002) Introduction: anthrax history, disease and ecology. Curr Top Microbiol Immunol 271: 1-19.
2. Madani N, Mendy C, Moutou F, Garin-Bastuji B (2010) La fièvre charbonneuse en France. Épisodes de l'été 2009 et foyers enregistrés sur la dernière décennie (1999-2009). Bulletin épidémiologique hebdomadaire.
3. Anaraki S, Addiman S, Nixon G, Krahe D, Ghosh R, et al. (2008) Investigations and control measures following a case of inhalation anthrax in East London in a drum maker and drummer, October 2008. Euro Surveill 13.
4. CDC (2010) Gastrointestinal anthrax after an animal-hide drumming event - New Hampshire and Massachusetts, 2009. MMWR Morb Mortal Wkly Rep 59: 872-877.
5. Keim P, Gruendike JM, Klevytska AM, Schupp JM, Challacombe J, et al. (2009) The genome and variation of Bacillus anthracis. Mol Aspects Med 30: 397-405.
6. Keim P, Price LB, Klevytska AM, Smith KL, Schupp JM, et al. (2000) Multiplelocus variable-number tandem repeat analysis reveals genetic relationships within Bacillus anthracis. J Bacteriol 182: 2928-2936. (Pubitemid 30246926)
7. Pearson T, Busch JD, Ravel J, Read TD, Rhoton SD, et al. (2004) Phylogenetic discovery bias in Bacillus anthracis using single-nucleotide polymorphisms from whole-genome sequencing. Proc Natl Acad Sci U S A 101: 13536-13541. (Pubitemid 39238438)
8. Van Ert MN, Easterday WR, Huynh LY, Okinaka RT, Hugh-Jones ME, et al. (2007) Global genetic population structure of Bacillus anthracis. PLoS One 2: e461.
9. Kenefic LJ, Pearson T, Okinaka RT, Schupp JM, Wagner DM, et al. (2009) Pre- Columbian origins for North American anthrax. PLoS One 4: e4813.
10. Le Flèche P, Hauck Y, Onteniente L, Prieur A, Denoeud F, et al. (2001) A tandem repeats database for bacterial genomes: application to the genotyping of Yersinia pestis and Bacillus anthracis. BMC Microbiol 1: 2.
11. Lista F, Faggioni G, Valjevac S, Ciammaruconi A, Vaissaire J, et al. (2006) Genotyping of Bacillus anthracis strains based on automated capillary 25-loci multiple locus variable-number tandem repeats analysis. BMC Microbiol 6: 33.
12. Okutani A, Sekizuka T, Boldbaatar B, Yamada A, Kuroda M, et al. (2010) 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 72: 93-97.
13. Pilo P, Perreten V, Frey J (2008) Molecular epidemiology of Bacillus anthracis: determining the correct origin. Appl Environ Microbiol 74: 2928-2931. (Pubitemid 351632626)
14. Stratilo CW, Lewis CT, Bryden L, Mulvey MR, Bader D (2006) Single-nucleotide repeat analysis for subtyping Bacillus anthracis isolates. J Clin Microbiol 44: 777-782.
15. Keim P, Van Ert MN, Pearson T, Vogler AJ, Huynh LY, et al. (2004) Anthrax molecular epidemiology and forensics: using the appropriate marker for different evolutionary scales. Infect Genet Evol 4: 205-213. (Pubitemid 39185926)
16. Beyer W, Bellan S, Eberle G, Ganz HH, Getz WM, et al. (2012) Distribution and molecular evolution of Bacillus anthracis genotypes in Namibia. PLoS Negl Trop Dis 6: e1534.
17. Fouet A, Smith KL, Keys C, Vaissaire J, Le Doujet C, et al. (2002) Diversity among French Bacillus anthracis isolates. J Clin Microbiol 40: 4732-4734. (Pubitemid 35434975)
18. Patra G, Vaissaire J, Weber-Levy M, Le Doujet C, Mock M (1998) Molecular characterization of Bacillus strains involved in outbreaks of anthrax in France in 1997. J Clin Microbiol 36: 3412-3414. (Pubitemid 28476209)
19. Gierczynski R, Kaluzewski S, Rakin A, Jagielski M, Zasada A, et al. (2004) Intriguing diversity of Bacillus anthracis in eastern Poland-the molecular echoes of the past outbreaks. FEMS Microbiol Lett 239: 235-240. (Pubitemid 39346130)
20. Fasanella A, Van Ert M, Altamura SA, Garofolo G, Buonavoglia C, et al. (2005) Molecular diversity of Bacillus anthracis in Italy. J Clin Microbiol 43: 3398-3401. (Pubitemid 40981353)
21. Maho A, Rossano A, Hachler H, Holzer A, Schelling E, et al. (2006) Antibiotic susceptibility and molecular diversity of Bacillus anthracis strains in Chad: detection of a new phylogenetic subgroup. J Clin Microbiol 44: 3422-3425. (Pubitemid 44413795)
22. Smith KL, DeVos V, Bryden H, Price LB, Hugh-Jones ME, et al. (2000) Bacillus anthracis diversity in Kruger National Park. J Clin Microbiol 38: 3780-3784.
23. Durmaz R, Doganay M, Sahin M, Percin D, Karahocagil MK, et al. (2012) Molecular epidemiology of the Bacillus anthracis isolates collected throughout Turkey from 1983 to 2011. Eur J Clin Microbiol Infect Dis 31: 2783-2790.
24. Merabishvili M, Natidze M, Rigvava S, Brusetti L, Raddadi N, et al. (2006) Diversity of Bacillus anthracis strains in Georgia and of vaccine strains from the former Soviet Union. Appl Environ Microbiol 72: 5631-5636.
25. Stratilo CW, Bader DE (2012) Genetic diversity among Bacillus anthracis soil isolates at fine geographic scales. Appl Environ Microbiol 78: 6433-6437.
26. Antwerpen M, Ilin D, Georgieva E, Meyer H, Savov E, et al. (2011) MLVA and SNP analysis identified a unique genetic cluster in Bulgarian Bacillus anthracis strains. Eur J Clin Microbiol Infect Dis 30: 923-930.
27. Sue D, Marston CK, Hoffmaster AR, Wilkins PP (2007) Genetic diversity in a Bacillus anthracis historical collection (1954 to 1988). J Clin Microbiol 45: 1777-1782. (Pubitemid 46933906)
28. Denoeud F, Vergnaud G (2004) Identification of polymorphic tandem repeats by direct comparison of genome sequence from different bacterial strains: a web-based resource. BMC Bioinformatics 5: 4.
29. Grissa I, Bouchon P, Pourcel C, Vergnaud G (2008) On-line resources for bacterial micro-evolution studies using MLVA or CRISPR typing. Biochimie 90: 660-668.
30. Hoffmaster AR, Fitzgerald CC, Ribot E, Mayer LW, Popovic T (2002) Molecular subtyping of Bacillus anthracis and the 2001 bioterrorism-associated anthrax outbreak, United States. Emerg Infect Dis 8: 1111-1116. (Pubitemid 35257003)
31. Cheung DT, Kam KM, Hau KL, Au TK, Marston CK, et al. (2005) 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 43: 1992-1994.
32. Ryu C, Lee K, Hawng HJ, Yoo CK, Seong WK, et al. (2005) Molecular characterization of Korean Bacillus anthracis isolates by amplified fragment length polymorphism analysis and multilocus variable-number tandem repeat analysis. Appl Environ Microbiol 71: 4664-4671. (Pubitemid 41129523)
33. Visca P, D'Arezzo S, Ramisse F, Gelfand Y, Benson G, et al. (2011) Investigation of the Legionella pneumophila population structure by analysis of tandem repeat copy number and internal sequence variation. Microbiology.
34. Hunter PR, Gaston MA (1988) Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J Clin Microbiol 26: 2465-2466.
35. Haubold B, Hudson RR (2000) LIAN 3.0: detecting linkage disequilibrium in multilocus data. Linkage Analysis. Bioinformatics 16: 847-848.
36. O'Sullivan MV, Sintchenko V, Gilbert GL (2013) Software for selecting the most informative sets of genomic loci for multi-target microbial typing. BMC Bioinformatics 14: 148.
37. Le Flèche P, Fabre M, Denoeud F, Koeck JL, Vergnaud G (2002) High resolution, on-line identification of strains from the Mycobacterium tuberculosis complex based on tandem repeat typing. BMC Microbiol 2: 37.
38. Drevet C, Pourcel C (2012) How to identify CRISPRs in sequencing data. Methods Mol Biol 905: 15-27.
39. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
40. Derzelle S, Laroche S, Le Flèche P, Hauck Y, Thierry S, et al. (2011) Characterization of genetic diversity of Bacillus anthracis in France by using high-resolution melting assays and multilocus variable-number tandem-repeat analysis. J Clin Microbiol 49: 4286-4292.
41. Kilic S, Ivanov IN, Durmaz R, Bayraktar MR, Ayaslioglu E, et al. (2011) Multiple-locus variable-number tandem-repeat analysis genotyping of human Brucella isolates from Turkey. J Clin Microbiol 49: 3276-3283.
42. Birdsell DN, Pearson T, Price EP, Hornstra HM, Nera RD, et al. (2012) Melt analysis of mismatch amplification mutation assays (Melt-MAMA): a functional study of a cost-effective SNP genotyping assay in bacterial models. PLoS One 7: e32866.
43. Leski TA, Caswell CC, Pawlowski M, Klinke DJ, Bujnicki JM, et al. (2009) 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 75: 7163-7172.
44. Sobral D, Le Cann P, Gerard A, Jarraud S, Lebeau B, et al. (2011) High-throughput typing method to identify a non-outbreak-involved Legionella pneumophila strain colonizing the entire water supply system in the town of Rennes, France. Appl Environ Microbiol 77: 6899-6907.
45. Sobral D, Mariani-Kurkdjian P, Bingen E, Vu-Thien H, Hormigos K, et al. (2012) A new highly discriminatory multiplex capillary-based MLVA assay as a tool for the epidemiological survey of Pseudomonas aeruginosa in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis 31: 2247-2256.
46. Larkeryd A, Myrtennas K, Karlsson E, Dwibedi CK, Forsman M, et al. (2014) CanSNPer: a hierarchical genotype classifier of clonal pathogens. Bioinformatics.
47. Karlsson E, Macellaro A, Bystrom M, Forsman M, Frangoulidis D, et al. (2014) Eight New Genomes and Synthetic Controls Increase the Accessibility of Rapid Melt-MAMA SNP Typing of Coxiella burnetii. PLoS One 9: e85417.