Diversity of group i and II clostridium botulinum strains from France including recently identified subtypes

Genome Biology and Evolution

Volumn 8, Issue 6, 2016, Pages 1643-1660

  Mazuet, Christelle ^a   Legeay, Christine ^a   Sautereau, Jean ^a   Ma, Laurence ^a   Bouchier, Christiane ^a   Bouvet, Philippe ^a   Popoff, Michel R ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

Botulism; Clostridium botulinum; Multilocus sequence typing; Whole genome sequencing

Indexed keywords

BOTULISM; CLASSIFICATION; CLOSTRIDIUM BOTULINUM; DNA SEQUENCE; FRANCE; GENETIC VARIATION; GENETICS; HUMAN; MICROBIOLOGY; MOLECULAR EVOLUTION; MULTILOCUS SEQUENCE TYPING; PATHOGENICITY; PHYLOGENY;

BOTULISM; CLOSTRIDIUM BOTULINUM; EVOLUTION, MOLECULAR; FRANCE; GENETIC VARIATION; HUMANS; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

EID: 84991801377     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evw101     Document Type: Article

References (78)

1. Aureli P, Franciosa G, Fenicia L. 2002. Infant botulism and honey in Europe: A commentary. Pediatr Infect Dis J. 21:866-868.
2. Barash JR, Arnon SS. 2014. A novel strain of Clostridium botulinum that produces type B and type H botulinum toxins. J Infect Dis. 209:183-191. doi: 110.1093/infdis/jit1449. Epub 2013 Oct 1097.
3. Becher F, Duriez E, Volland H, Tabet JC, Ezan E. 2007. Detection of functional ricin by immunoaffinity and liquid chromatography-tandem mass spectrometry. Anal Chem. 79:659-665.
4. Bowmer EJ. 1963. Preparation and assay of the international standards for Clostridium botulinum types a, B, C, D and E antitoxins. Bull World Health Organ 29:701-709.
5. Brüggemann H, Wollherr A, Mazuet C, Popoff MR. 2011. Clostridium botulinum. In: Fratamico P, Liu Y, Kathariou S, editors. Genomes of foodborne and waterborne pathogens Washington (DC): ASM Press. p. 185-212.
6. Carlier JP, Espié E, Popoff MR. 2007. Le botulisme en France, 2003-2006. Bull Epidemiol. 31-32:281-284.
7. Carter AT, et al. 2010. Further characterization of proteolytic Clostridium botulinum type A5 reveals that neurotoxin formation is unaffected by loss of the cntR (botR) promoter sigma factor binding site. J Clin Microbiol. 48:1012-1013.
8. Carter AT, et al. 2011. Complete genome sequence of the proteolytic Clostridium botulinum type A5 (B30) strain H04402 065. J Bacteriol. 193:2351-2352.
9. Carter AT, Peck MW. 2015. Genomes, neurotoxins and biology of Clostridium botulinum Group I and Group II. Res Microbiol. 166:303-317.
10. Dahlenborg M, Borch E, Radstrom P. 2001. Development of a combined selection and enrichment PCR procedure for Clostridium botulinum Types B, E, and F and its use to determine prevalence in fecal samples from slaughtered pigs. Appl Environ Microbiol. 67:4781-4788.
11. Dineen SS, Bradshaw M, Johnson EA. 2003. Neurotoxin gene clusters in Clostridium botulinum type A strains: Sequence comparison and evolutionary implications. Curr Microbiol. 46:342-352.
12. Dover N, Barash JR, Arnon SS. 2010. Identical novel A5(B30 ) botulinum neurotoxin gene arrangements isolated from widely disparate geographical and patient sources suggest their independent origins. J Clin Microbiol. 48:1989.
13. Dover N, Barash JR, Hill KK, Xie G, Arnon SS. 2014. Molecular characterization of a novel botulinum neurotoxin type H gene. J Infect Dis. 209:192-202.
14. Eleopra R, Tugnoli V, Rossetto O, De Grandis D, Montecucco C. 1998. Different time courses of recovery after poisoning with botulinum neurotoxin serotypes A and E in humans. Neurosci Lett. 256:135-138.
15. Foran PG, et al. 2003. Evaluation of the therapeutic usefulness of botulinum neurotoxin B, C1, E and F compared with the long lasting type A. J Biol Chem. 278:1363-1371.
16. Franciosa G, Maugliani A, Scalfaro C, Aureli P. 2009. Evidence that plasmid-borne botulinum neurotoxin type B genes are widespread among Clostridium botulinum serotype B strains. PLoS One 4:e4829.
17. Giordani F, et al. 2015. Genomic characterization of Italian Clostridium botulinum group I strains. Infect Genet Evol. 36:62-71.
18. Gonzalez-Escalona N, Thirunavukkarasu N, et al. 2014. Draft genome sequence of bivalent Clostridium botulinum strain IBCA10-7060, encoding botulinum neurotoxin B and a new FA mosaic type. Genome Announc. 2(6):e01275-e01214.
19. Gonzalez-Escalona N, Timme R, Raphael BH, Zink D, Sharma SK. 2014. Whole-genome single-nucleotide-polymorphism analysis for discrimination of Clostridium botulinum group I strains. Appl Environ Microbiol. 80:2125-2132.
20. Hatheway CL, McCroskey LM, Lombard GL, Dowell VR Jr. 1981. Atypical toxin variant of Clostridium botulinum type B associated with infant botulism. J Clin Microbiol. 14:607-611.
21. Hill KK, et al. 2007. Genetic diversity among Botulinum neurotoxinproducing clostridial strains. J Bacteriol. 189:818-832.
22. Hill KK, et al. 2009. Recombination and insertion events involving the botulinum neurotoxin complex genes in Clostridium botulinum types A, B, E and F and Clostridium butyricum type E strains. BMC Biol. 7:66.
23. Hill KK, Smith TJ. 2013. Genetic diversity within Clostridium botulinum serotypes, botulinum neurotoxin gene clusters and toxin subtypes. Curr Top Microbiol Immunol. 364:1-20.
24. Hill KK, Xie G, Foley BT, Smith TJ. 2015. Genetic diversity within the botulinum neurotoxin-producing bacteria and their neurotoxins. Toxicon. 107:2-8.
25. Hughes JM, et al. 1981. Clinical features of types A and B food-borne botulism. Ann Intern Med 95:442-445.
26. Jacobson MJ, et al. 2011. Purification, modeling, and analysis of botulinum neurotoxin subtype A5 (BoNT/A5) from Clostridium botulinum strain A661222. Appl Environ Microbiol. 77:4217-4222.
27. Jacobson MJ, Lin G, Whittam TS, Johnson EA. 2008. Phylogenetic analysis of Clostridium botulinum type A by multi-locus sequence typing. Microbiology 154:2408-2415.
28. Jenzer G, MumenthalerM, Ludin HP, Robert F. 1975. Autonomic dysfunction in botulism B: A clinical report. Neurology 25:150-153.
29. Jousimies-Somer HR, et al. 2002. Anaerobic bacteriology manual. Belmont (CA): Star Publishing Company.
30. Keller JE. 2006. Recovery from botulinum neurotoxin poisoning in vivo. Neuroscience 139:629-637.
31. Keller JE, Neale EA, Oyler G, Adler M. 1999. Persistence of botulinum neurotoxin action in cultured spinal cord cells. FEBS Lett. 456:137-142.
32. Kenri T, et al. 2014. Genetic characterization and comparison of Clostridium botulinum strains isolated from botulism cases in Japan between 2006 and 2011. Appl Environ Microbiol. 5:02134-02114.
33. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 16:111-120.
34. King LA. 2008. Two severe cases of botulism associated with industrially produced chicken enchiladas, France, August 2008. Euro Surveill 13(37):1-2.
35. King LA, et al. 2009. Botulism and hot-smoked whitefish: A family cluster of type E botulism in France, September 2009. Euro Surveill 14(45): 1-3.
36. King LA, et al. 2010. Infant botulism in France, 1991-2009. Arch Pediatr. 17:1288-1292.
37. Koepke R, Sobel J, Arnon SS. 2008. Global occurrence of infant botulism, 1976-2006. Pediatrics 122:e73-e82.
38. Kull S, et al. 2015. Isolation and functional characterization of the novel Clostridium botulinum neurotoxin A8 subtype. PLoS One 10:e0116381.
39. Lindstrôm M, Kiviniemi K, Korkeala H. 2006. Hazard and control of group II (non-proteolytic) Clostridium botulinum in modern food processing. Int J Food Microbiol. 108:92-104.
40. Luquez C, et al. 2012. Genetic diversity among Clostridium botulinum strains harboring bont/A2 and bont/A3 genes. Appl Environ Microbiol. 78:8712-8718.
41. Macdonald TE, et al. 2011. Analysis of Clostridium botulinum serotype E strains by using multilocus sequence typing, amplified fragment length polymorphism, variable-number tandem-repeat analysis, and botulinum neurotoxin gene sequencing. Appl Environ Microbiol. 77:8625-8634.
42. Mazuet C, Bouchier C, Popoff MR. 2015. Draft genome sequence of Clostridium botulinum strain 277-00 type B2. Genome Announc 3.
43. Mazuet C, Sautereau J, et al. 2015. An atypical outbreak of food-borne botulism due to Clostridium botulinum types B and E from ham. J Clin Microbiol. 53:722-726.
44. Mazuet C, Bouvet P, King LA, Popoff MR. 2011. Le botulisme humain en France, 2007-2009. BEH 6:49-53.
45. Mazuet C, et al. 2014. Le botulisme humain en France, 2010-2012. BEH 6:106-114.
46. McCallum N, et al. 2015. Genomic epidemiology of Clostridium botulinum isolates from temporally related cases of infant botulism in New South Wales, Australia. J Clin Microbiol. 53:2846-2853.
47. Merz B, Bigalke H, Stoll G, Naumann M. 2003. Botulism type B presenting as pure autonomic dysfunction. Clin Auton Res. 13:337-338.
48. Meunier FA, Lisk G, Sesardic D, Dolly JO. 2003. Dynamics of motor nerve terminal remodeling unveiled using SNARE-cleaving botulinum toxins: The extent and duration are dictated by the sites of SNAP-25 truncation. Mol Cell Neurosci. 22:454-466.
49. Myllykoski J, Nevas M, Lindstrôm M, Korkeala H. 2006. The detection and prevalence of Clostridium botulinum in pig intestinal samples. Int J Food Microbiol. 110:172-177.
50. O'Sullivan GA, Mohammed N, Foran PG, Lawrence GW, Dolly JO. 1999. Rescue of exocytosis in botulinum toxin A-poisoned chromaffin cells by expression of cleavage-resistant SNAP-25. J Biol Chem. 274: 36897-36904.
51. Olsen JS, et al. 2014. Analysis of the genetic distribution among members of Clostridium botulinum group I using a novel multilocus sequence typing (MLST) assay. J Microbiol Methods 96:84-91.
52. Oriot C, et al. 2011. One collective case of type A foodborne botulism in Corsica. Clin Toxicol. (Phila) 49:752-754.
53. Peck MW, Stringer SC, Carter AT. 2011. Clostridium botulinum in the postgenomic era. Food Microbiol. 28:183-191.
54. Pier CL, et al. 2011. Botulinum neurotoxin subtype A2 enters neuronal cells faster than subtype A1. FEBS Lett. 595:199-206.
55. Pingeon J, et al. 2011. Two outbreaks of botulism associated with consumption of green olive paste, France, September 2011. Euro Surveill 16(49): 1-3.
56. Popoff MR. 1995. Ecology of neurotoxigenic strains of Clostridia. Curr Top Microbiol Immunol. 195:1-29.
57. Popoff MR, Bouvet P. 2013. Genetic characteristics of toxigenic Clostridia and toxin gene evolution Toxicon. 75, 63-89.
58. Potulska-Chromik A, et al. 2013. Long lasting dysautonomia due to botulinum toxin B poisoning: Clinical-laboratory follow up and difficulties in initial diagnosis. BMC Res Notes 6:438. 10.1186/1756-0500-1186-1438.
59. Pourshafie MR, et al. 1998. An outbreak of food-borne botulism associated with contaminated locallymade cheese in Iran. Scand J Infect Dis. 30:92-94.
60. Raphael BH, Shirey TB, Luquez C, Maslanka SE. 2014. Distinguishing highly-related outbreak-associated Clostridium botulinum type A(B) strains. BMC Microbiol. 14:192. 10.1186/1471-2180-1114-1192.
61. Skarin H, Segerman B. 2011. Horizontal gene transfer of toxin genes in Clostridium botulinum: Involvement of mobile elements and plasmids. Mob Genet Elements 1:213-215.
62. Smith TJ, et al. 2005. Sequence variation within botulinum neurotoxin serotypes impacts antibody binding and neutralization. Infect Immun. 73:5450-5457.
63. Smith TJ, Hill KK, Raphael BH. 2015. Historical and current perspectives on Clostridium botulinum diversity. Res Microbiol. 166:290-302.
64. Smith TJ, Hill KK, Xie G, et al. 2015. Genomic sequences of six botulinum neurotoxin-producing strains representing three clostridial species illustrate the mobility and diversity of botulinum neurotoxin genes. Infect Genet Evol. 30:102-113.
65. Sobel J. 2005. Botulism. Clin Infect Dis 41:1167-1173.
66. Stringer SC, et al. 2013. Genomic and physiological variabilitywithin Group II (non-proteolytic) Clostridium botulinum. BMC Genomics 14:333.
67. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 30:2725-2729.
68. There H. 1999. Le botulisme en Europe. Euro Surveill 4:2-7.
69. Torii Y, et al. 2011. Comparison of effects of botulinum toxin subtype A1 and A2 using twitch tension assay and rat grip strength test. Toxicon 57:93-99.
70. Torii Y, et al. 2013. Differences in immunological responses of polyclonal botulinum A1 and A2 antitoxin against A1 and A2 toxin. Toxicon 73:9-16.
71. Umeda K, Seto Y, Kohda T, Mukamoto M, Kozaki S. 2009. Genetic characterization of Clostridium botulinum associated with type B infant botulism in Japan. J Clin Microbiol. 47:2720-2728.
72. Umeda K, Wada T, Kohda T, Kozaki S. 2013. Multi-locus variable number tandem repeat analysis for Clostridium botulinum type B isolates in Japan: Comparison with other isolates and genotyping methods. Infect Genet Evol. 16:298-304.
73. Vanhomwegen J, et al. 2013. Application of high-density DNA resequencing microarray for detection and characterization of botulinum neurotoxin-producing clostridia. PLoS One 8:e67510.
74. Weedmark KA, et al. 2014. Whole genome sequencing of 175 Clostridium botulinum Type E strains reveals two novel toxin variants. Appl Environ Microbiol. 80:6334-6345.
75. Weedmark KA, et al. 2015. Clostridium botulinum group II isolate phylogenomic profiling using whole-genome sequence data. Appl Environ Microbiol. 81:5938-5948.
76. Whitemarsh RC, et al. 2013. Characterization of botulinum neurotoxin A subtypes 1 through 5 by investigation of activities in mice, in neuronal cell cultures, and in vitro. Infect Immun. 81:3894-3902.
77. Whitemarsh RC, Tepp WH, Johnson EA, Pellett S. 2014. Persistence of botulinum neurotoxin a subtypes 1-5 in primary rat spinal cord cells. PLoS One 9:e90252.
78. Williamson CH, et al. 2016. Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia. BMC Genomics 17:180.