publication . Article . 2017

Differentiating Botulinum Neurotoxin-Producing Clostridia with a Simple, Multiplex PCR Assay

Williamson, Charles H. D.; Vazquez, Adam J.; Hill, Karen; Smith, Theresa J.; Nottingham, Roxanne; Stone, Nathan E.; Sobek, Colin J.; Cocking, Jill H.; Fernández, Rafael A.; Caballero, Patricia A.; ...
Open Access English
  • Published: 01 Aug 2017 Journal: Applied and Environmental Microbiology, volume 83, issue 18 (issn: 0099-2240, eissn: 1098-5336, Copyright policy)
  • Publisher: American Society for Microbiology
Abstract
ABSTRACT Diverse members of the genus Clostridium produce botulinum neurotoxins (BoNTs), which cause a flaccid paralysis known as botulism. While multiple species of clostridia produce BoNTs, the majority of human botulism cases have been attributed to Clostridium botulinum groups I and II. Recent comparative genomic studies have demonstrated the genomic diversity within these BoNT-producing species. This report introduces a multiplex PCR assay for differentiating members of C. botulinum group I, C. sporogenes, and two major subgroups within C. botulinum group II. Coding region sequences unique to each of the four species/subgroups were identified by in silico a...
Subjects
free text keywords: Clostridium botulinum, Methods, whole-genome sequencing, biomarker, PCR
88 references, page 1 of 6

1.Collins MD, East AK 1998 Phylogeny and taxonomy of the food-borne pathogen Clostridium botulinum and its neurotoxins. J Appl Microbiol 84:5–17. doi:10.1046/j.1365-2672.1997.00313.x.15244052 [PubMed] [DOI]

2.Smith TJ, Hill KK, Raphael BH 2015 Historical and current perspectives on Clostridium botulinum diversity. Res Microbiol 166:290–302. doi:10.1016/j.resmic.2014.09.007.25312020 [PubMed] [DOI]

3.Dahlsten E, Lindström M, Korkeala H 2015 Mechanisms of foo d processing and storage-related stress tolerance in Clostridium botulinum. Res Microbiol 166:344–352. doi:10.1016/j.resmic.2014.09.011.25303833 [PubMed] [DOI]

4.Eklund MW, Poysky FT, Wieler DI 1967 Characteristics of Clostridium botulinum Type F isolated from the Pacific Coast of the United States. Appl Microbiol 15:1316–1323.4865980 [OpenAIRE] [PubMed]

5.Eklund MW, Wieler DI, Poysky FT 1967 Outgrowth and toxin production of nonproteolytic type B Clostridium botulinum at 3.3 to 5.6 C. J Bacteriol 93:1461–1462.5340312 [OpenAIRE] [PubMed]

6.Graham AF, Mason DR, Maxwell FJ, Peck MW 1997 Effect of pH and NaCl on growth from spores of non-proteolytic Clostridium botulinum at chill temperature. Lett Appl Microbiol 24:95–100. doi:10.1046/j.1472-765X.1997.00348.x.9081311 [PubMed] [DOI]

7.Lindström 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. doi:10.1016/j.ijfoodmicro.2005.11.003.16480785 [PubMed] [DOI]

8.Peck MW, Goodburn KE, Betts RP, Stringer SC 2008 Assessment of the potential for growth and neurotoxin formation by non-proteolytic Clostridium botulinum in short shelf-life commercial foods designed to be stored chilled. Trends Food Sci Technol 19:207–216. doi:10.1016/j.tifs.2007.12.006. [DOI]

9.Hill KK, Smith TJ, Helma CH, Ticknor LO, Foley BT, Svensson RT, Brown JL, Johnson EA, Smith LA, Okinaka RT, Jackson PJ, Marks JD 2007 Genetic diversity among botulinum neurotoxin-producing clostridial strains. J Bacteriol 189:818–832. doi:10.1128/JB.01180-06.17114256 [OpenAIRE] [PubMed] [DOI]

10.Hill KK, Xie G, Foley BT, Smith TJ, Munk AC, Bruce D, Smith LA, Brettin TS, Detter JC 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. doi:10.1186/1741-7007-7-66.19804621 [OpenAIRE] [PubMed] [DOI]

11.Rossetto O, Pirazzini M, Montecucco C 2014 Botulinum neurotoxins: genetic, structural and mechanistic insights. Nat Rev Microbiol 12:535–549. doi:10.1038/nrmicro3295.24975322 [PubMed] [DOI]

12.Weigand MR, Pena-Gonzalez A, Shirey TB, Broeker RG, Ishaq MK, Konstantinidis KT, Raphael BH 2015 Implications of genome-based discrimination between Clostridium botulinum group I and Clostridium sporogenes strains for bacterial taxonomy. Appl Environ Microbiol 81:5420–5429. doi:10.1128/AEM.01159-15.26048939 [OpenAIRE] [PubMed] [DOI]

13.Williamson CHD, Sahl JW, Smith TJ, Xie G, Foley BT, Smith LA, Fernández RA, Lindström M, Korkeala H, Keim P, Foster J, Hill K 2016 Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing clostridia. BMC Genomics 17:180. doi:10.1186/s12864-016-2502-z.26939550 [OpenAIRE] [PubMed] [DOI]

14.Carter AT, Peck MW 2015 Genomes, neurotoxins and biology of Clostridium botulinum group I and group II. Res Microbiol 166:303–317. doi:10.1016/j.resmic.2014.10.010.25445012 [OpenAIRE] [PubMed] [DOI]

15.Koepke R, Sobel J, Arnon SS 2008 Global occurrence of infant botulism, 1976–2006. Pediatrics 122:e73–e82. doi:10.1542/peds.2007-1827.18595978 [PubMed] [DOI]

88 references, page 1 of 6
Abstract
ABSTRACT Diverse members of the genus Clostridium produce botulinum neurotoxins (BoNTs), which cause a flaccid paralysis known as botulism. While multiple species of clostridia produce BoNTs, the majority of human botulism cases have been attributed to Clostridium botulinum groups I and II. Recent comparative genomic studies have demonstrated the genomic diversity within these BoNT-producing species. This report introduces a multiplex PCR assay for differentiating members of C. botulinum group I, C. sporogenes, and two major subgroups within C. botulinum group II. Coding region sequences unique to each of the four species/subgroups were identified by in silico a...
Subjects
free text keywords: Clostridium botulinum, Methods, whole-genome sequencing, biomarker, PCR
88 references, page 1 of 6

1.Collins MD, East AK 1998 Phylogeny and taxonomy of the food-borne pathogen Clostridium botulinum and its neurotoxins. J Appl Microbiol 84:5–17. doi:10.1046/j.1365-2672.1997.00313.x.15244052 [PubMed] [DOI]

2.Smith TJ, Hill KK, Raphael BH 2015 Historical and current perspectives on Clostridium botulinum diversity. Res Microbiol 166:290–302. doi:10.1016/j.resmic.2014.09.007.25312020 [PubMed] [DOI]

3.Dahlsten E, Lindström M, Korkeala H 2015 Mechanisms of foo d processing and storage-related stress tolerance in Clostridium botulinum. Res Microbiol 166:344–352. doi:10.1016/j.resmic.2014.09.011.25303833 [PubMed] [DOI]

4.Eklund MW, Poysky FT, Wieler DI 1967 Characteristics of Clostridium botulinum Type F isolated from the Pacific Coast of the United States. Appl Microbiol 15:1316–1323.4865980 [OpenAIRE] [PubMed]

5.Eklund MW, Wieler DI, Poysky FT 1967 Outgrowth and toxin production of nonproteolytic type B Clostridium botulinum at 3.3 to 5.6 C. J Bacteriol 93:1461–1462.5340312 [OpenAIRE] [PubMed]

6.Graham AF, Mason DR, Maxwell FJ, Peck MW 1997 Effect of pH and NaCl on growth from spores of non-proteolytic Clostridium botulinum at chill temperature. Lett Appl Microbiol 24:95–100. doi:10.1046/j.1472-765X.1997.00348.x.9081311 [PubMed] [DOI]

7.Lindström 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. doi:10.1016/j.ijfoodmicro.2005.11.003.16480785 [PubMed] [DOI]

8.Peck MW, Goodburn KE, Betts RP, Stringer SC 2008 Assessment of the potential for growth and neurotoxin formation by non-proteolytic Clostridium botulinum in short shelf-life commercial foods designed to be stored chilled. Trends Food Sci Technol 19:207–216. doi:10.1016/j.tifs.2007.12.006. [DOI]

9.Hill KK, Smith TJ, Helma CH, Ticknor LO, Foley BT, Svensson RT, Brown JL, Johnson EA, Smith LA, Okinaka RT, Jackson PJ, Marks JD 2007 Genetic diversity among botulinum neurotoxin-producing clostridial strains. J Bacteriol 189:818–832. doi:10.1128/JB.01180-06.17114256 [OpenAIRE] [PubMed] [DOI]

10.Hill KK, Xie G, Foley BT, Smith TJ, Munk AC, Bruce D, Smith LA, Brettin TS, Detter JC 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. doi:10.1186/1741-7007-7-66.19804621 [OpenAIRE] [PubMed] [DOI]

11.Rossetto O, Pirazzini M, Montecucco C 2014 Botulinum neurotoxins: genetic, structural and mechanistic insights. Nat Rev Microbiol 12:535–549. doi:10.1038/nrmicro3295.24975322 [PubMed] [DOI]

12.Weigand MR, Pena-Gonzalez A, Shirey TB, Broeker RG, Ishaq MK, Konstantinidis KT, Raphael BH 2015 Implications of genome-based discrimination between Clostridium botulinum group I and Clostridium sporogenes strains for bacterial taxonomy. Appl Environ Microbiol 81:5420–5429. doi:10.1128/AEM.01159-15.26048939 [OpenAIRE] [PubMed] [DOI]

13.Williamson CHD, Sahl JW, Smith TJ, Xie G, Foley BT, Smith LA, Fernández RA, Lindström M, Korkeala H, Keim P, Foster J, Hill K 2016 Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing clostridia. BMC Genomics 17:180. doi:10.1186/s12864-016-2502-z.26939550 [OpenAIRE] [PubMed] [DOI]

14.Carter AT, Peck MW 2015 Genomes, neurotoxins and biology of Clostridium botulinum group I and group II. Res Microbiol 166:303–317. doi:10.1016/j.resmic.2014.10.010.25445012 [OpenAIRE] [PubMed] [DOI]

15.Koepke R, Sobel J, Arnon SS 2008 Global occurrence of infant botulism, 1976–2006. Pediatrics 122:e73–e82. doi:10.1542/peds.2007-1827.18595978 [PubMed] [DOI]

88 references, page 1 of 6
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