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Title: Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia

Abstract

Background: Clostridium botulinum is a diverse group of bacteria characterized by the production of botulinum neurotoxin. Botulinum neurotoxins are classified into serotypes (BoNT/A–G), which are produced by six species/Groups of Clostridia, but the genetic background of the bacteria remains poorly understood. The purpose of this study was to use comparative genomics to provide insights into the genetic diversity and evolutionary history of bacteria that produce the potent botulinum neurotoxin. Results: Comparative genomic analyses of over 170 Clostridia genomes, including our draft genome assemblies for 59 newly sequenced Clostridia strains from six continents and publicly available genomic data, provided in-depth insights into the diversity and distribution of BoNT-producing bacteria. These newly sequenced strains included Group I and II strains that express BoNT/A,/B,/E, or/F as well as bivalent strains. BoNT-producing Clostridia and closely related Clostridia species were delineated with a variety of methods including 16S rRNA gene, concatenated marker genes, core genome and concatenated multi-locus sequencing typing (MLST) gene phylogenies that related whole genome sequenced strains to publicly available strains and sequence types. These analyses illustrated the phylogenetic diversity in each Group and the diversity of genomic backgrounds that express the same toxin type or subtype. Comparisons of the botulinum neurotoxin genesmore » did not identify novel toxin types or variants. Conclusions: This study represents one of the most comprehensive analyses of whole genome sequence data for Group I and II BoNT-producing strains. Read data and draft genome assemblies generated for 59 isolates will be a resource to the research community. Core genome phylogenies proved to be a powerful tool for differentiating BoNT-producing strains and can provide a framework for the study of these bacteria. Comparative genomic analyses of Clostridia species illustrate the diversity of botulinum-neurotoxin-producing strains and the plasticity of the genomic backgrounds in which bont genes are found.« less

Authors:
 [1];  [1];  [2];  [3];  [4];  [5];  [6];  [7];  [7];  [1];  [1];  [3]
  1. Northern Arizona Univ., Flagstaff, AZ (United States). Center for Microbial Genetics and Genomics
  2. US Army Medical Research Inst. of Infectious Diseases, Fort Detrick, MD (United States)
  3. Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Bioscience Div.
  4. Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Div.
  5. US Army Medical Research Inst of Infecgious Diseases, Fort Detrick, MD (United States). Medical Countermeasures Technology, US Army Medical Research and Material Command
  6. Área Microbiología, Departamento de Patología, Facultad de Ciencias Médicas, Universidad Nacional de Cuyo, Centro Universitario, Mendoza (Argentina)
  7. Univ. of Helsinki (Finland). Dept. of Food Hygiene and Environmental Health
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE; U.S. Department of Homeland Security
OSTI Identifier:
1626797
Grant/Contract Number:  
AC52-06NA25396; HSHQDC-10-C-00139; DHS-2010-ST-108-000019
Resource Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 17; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biotechnology & Applied Microbiology; Genetics & Heredity; Clostridium botulinum; Botulinum neurotoxin; Whole genome sequence; Comparative

Citation Formats

Williamson, Charles H. D., Sahl, Jason W., Smith, Theresa J., Xie, Gary, Foley, Brian T., Smith, Leonard A., Fernández, Rafael A., Lindström, Miia, Korkeala, Hannu, Keim, Paul, Foster, Jeffrey, and Hill, Karen. Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia. United States: N. p., 2016. Web. doi:10.1186/s12864-016-2502-z.
Williamson, Charles H. D., Sahl, Jason W., Smith, Theresa J., Xie, Gary, Foley, Brian T., Smith, Leonard A., Fernández, Rafael A., Lindström, Miia, Korkeala, Hannu, Keim, Paul, Foster, Jeffrey, & Hill, Karen. Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia. United States. https://doi.org/10.1186/s12864-016-2502-z
Williamson, Charles H. D., Sahl, Jason W., Smith, Theresa J., Xie, Gary, Foley, Brian T., Smith, Leonard A., Fernández, Rafael A., Lindström, Miia, Korkeala, Hannu, Keim, Paul, Foster, Jeffrey, and Hill, Karen. Thu . "Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia". United States. https://doi.org/10.1186/s12864-016-2502-z. https://www.osti.gov/servlets/purl/1626797.
@article{osti_1626797,
title = {Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia},
author = {Williamson, Charles H. D. and Sahl, Jason W. and Smith, Theresa J. and Xie, Gary and Foley, Brian T. and Smith, Leonard A. and Fernández, Rafael A. and Lindström, Miia and Korkeala, Hannu and Keim, Paul and Foster, Jeffrey and Hill, Karen},
abstractNote = {Background: Clostridium botulinum is a diverse group of bacteria characterized by the production of botulinum neurotoxin. Botulinum neurotoxins are classified into serotypes (BoNT/A–G), which are produced by six species/Groups of Clostridia, but the genetic background of the bacteria remains poorly understood. The purpose of this study was to use comparative genomics to provide insights into the genetic diversity and evolutionary history of bacteria that produce the potent botulinum neurotoxin. Results: Comparative genomic analyses of over 170 Clostridia genomes, including our draft genome assemblies for 59 newly sequenced Clostridia strains from six continents and publicly available genomic data, provided in-depth insights into the diversity and distribution of BoNT-producing bacteria. These newly sequenced strains included Group I and II strains that express BoNT/A,/B,/E, or/F as well as bivalent strains. BoNT-producing Clostridia and closely related Clostridia species were delineated with a variety of methods including 16S rRNA gene, concatenated marker genes, core genome and concatenated multi-locus sequencing typing (MLST) gene phylogenies that related whole genome sequenced strains to publicly available strains and sequence types. These analyses illustrated the phylogenetic diversity in each Group and the diversity of genomic backgrounds that express the same toxin type or subtype. Comparisons of the botulinum neurotoxin genes did not identify novel toxin types or variants. Conclusions: This study represents one of the most comprehensive analyses of whole genome sequence data for Group I and II BoNT-producing strains. Read data and draft genome assemblies generated for 59 isolates will be a resource to the research community. Core genome phylogenies proved to be a powerful tool for differentiating BoNT-producing strains and can provide a framework for the study of these bacteria. Comparative genomic analyses of Clostridia species illustrate the diversity of botulinum-neurotoxin-producing strains and the plasticity of the genomic backgrounds in which bont genes are found.},
doi = {10.1186/s12864-016-2502-z},
journal = {BMC Genomics},
number = 1,
volume = 17,
place = {United States},
year = {Thu Mar 03 00:00:00 EST 2016},
month = {Thu Mar 03 00:00:00 EST 2016}
}

Journal Article:
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Figures / Tables:

Table 1 Table 1: Information regarding newly sequenced strains

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Works referenced in this record:

DNest4: Diffusive Nested Sampling in C++ and Python
preprint, January 2016


Shifting the genomic gold standard for the prokaryotic species definition
journal, October 2009

  • Richter, Michael; Rosselló-Móra, Ramon
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 45
  • DOI: 10.1073/pnas.0906412106

Phylogeny and taxonomy of the food-borne pathogen Clostridium botulinum and its neurotoxins
journal, January 1998


Effect of pH and NaCl on growth from spores of non‐proteolytic Clostridium botulinum at chill temperature
journal, February 1997


Phylogenetic analysis of Clostridium botulinum type A by multi-locus sequence typing
journal, August 2008


Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009


Food Microbiology
book, December 2012


Evidence that Plasmid-Borne Botulinum Neurotoxin Type B Genes Are Widespread among Clostridium botulinum Serotype B Strains
journal, March 2009


The species concept for prokaryotes
journal, January 2001


The Northern Arizona SNP Pipeline (NASP): accurate, flexible, and rapid identification of SNPs in WGS datasets
posted_content, January 2016

  • Sahl, Jason W.; Lemmer, Darrin; Travis, Jason
  • Microbial Genomics
  • DOI: 10.1101/037267

BIGSdb: Scalable analysis of bacterial genome variation at the population level
journal, December 2010


FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010


Commensal Pseudomonas protect Arabidopsis thaliana from a coexisting pathogen via multiple lineage-dependent mechanisms
journal, December 2021


Climatic oscillations in Quaternary have shaped the co-evolutionary patterns between the Norway spruce and its host-associated herbivore
journal, October 2020


Saccorhytus is an early ecdysozoan and not the earliest deuterostome
journal, August 2022


A novel algorithm and web-based tool for comparing two alternative phylogenetic trees
journal, October 2005


Food Microbiology
journal, November 1959


The large-scale blast score ratio (LS-BSR) pipeline: a method to rapidly compare genetic content between bacterial genomes
journal, January 2014

  • Sahl, Jason W.; Caporaso, J. Gregory; Rasko, David A.
  • PeerJ, Vol. 2
  • DOI: 10.7717/peerj.332

Mating pair stabilization mediates bacterial conjugation species specificity
journal, June 2022


GenBank
journal, December 2004

  • Benson, D. A.
  • Nucleic Acids Research, Vol. 33, Issue Database issue
  • DOI: 10.1093/nar/gki063

SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012

  • Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
  • Journal of Computational Biology, Vol. 19, Issue 5
  • DOI: 10.1089/cmb.2012.0021

Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

  • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
  • DOI: 10.1128/AEM.01541-09

Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

Analysis of a unique Clostridium botulinum strain from the Southern hemisphere producing a novel type E botulinum neurotoxin subtype
journal, January 2012

  • Raphael, Brian H.; Lautenschlager, Matthew; Kalb, Suzanne R.
  • BMC Microbiology, Vol. 12, Issue 1
  • DOI: 10.1186/1471-2180-12-245

Botulinum Toxin as a Biological Weapon: Medical and Public Health Management
journal, February 2001


A Rapid Bootstrap Algorithm for the RAxML Web Servers
journal, October 2008

  • Stamatakis, Alexandros; Hoover, Paul; Rougemont, Jacques
  • Systematic Biology, Vol. 57, Issue 5
  • DOI: 10.1080/10635150802429642

Clostridium botulinum group III: a group with dual identity shaped by plasmids, phages and mobile elements
journal, April 2011


Presence of Clostridium botulinum spores in Matricaria chamomilla (chamomile) and its relationship with infant botulism
journal, February 2008


Functional Characterization of Botulinum Neurotoxin Serotype H as a Hybrid of Known Serotypes F and A (BoNT F/A)
journal, March 2015

  • Kalb, Suzanne R.; Baudys, Jakub; Raphael, Brian H.
  • Analytical Chemistry, Vol. 87, Issue 7
  • DOI: 10.1021/ac504716v

Matplotlib: A 2D Graphics Environment
journal, January 2007


Environmental dissemination of pathogenic Listeria monocytogenes in flowing surface waters in Switzerland
journal, April 2021


Accurate and universal delineation of prokaryotic species
journal, July 2013

  • Mende, Daniel R.; Sunagawa, Shinichi; Zeller, Georg
  • Nature Methods, Vol. 10, Issue 9
  • DOI: 10.1038/nmeth.2575

A user's guide to microbial challenge testing for ensuring the safety and stability of food products
journal, April 1993


How Many Bootstrap Replicates Are Necessary?
journal, March 2010

  • Pattengale, Nicholas D.; Alipour, Masoud; Bininda-Emonds, Olaf R. P.
  • Journal of Computational Biology, Vol. 17, Issue 3
  • DOI: 10.1089/cmb.2009.0179

Historical and current perspectives on Clostridium botulinum diversity
journal, May 2015


Isolation and Functional Characterization of the Novel Clostridium botulinum Neurotoxin A8 Subtype
journal, February 2015


QUAST: quality assessment tool for genome assemblies
journal, February 2013


Evidence that Plasmid-Borne Botulinum Neurotoxin Type B Genes Are Widespread among Clostridium botulinum Serotype B Strains
journal, March 2009


Comparison of Clostridium botulinum genomes shows the absence of cold shock protein coding genes in type E neurotoxin producing strains
journal, January 2013

  • Söderholm, Henna; Jaakkola, Kaisa; Somervuo, Panu
  • The Botulinum J., Vol. 2, Issue 3/4
  • DOI: 10.1504/TBJ.2013.055662

High prevalence of Clostridium botulinum types A and B in honey samples detected by polymerase chain reaction
journal, January 2002

  • Nevas, Mari; Hielm, Sebastian; Lindström, Miia
  • International Journal of Food Microbiology, Vol. 72, Issue 1-2
  • DOI: 10.1016/S0168-1605(01)00615-8

Circos: An information aesthetic for comparative genomics
journal, June 2009


Shifting the genomic gold standard for the prokaryotic species definition
journal, October 2009

  • Richter, Michael; Rosselló-Móra, Ramon
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 45
  • DOI: 10.1073/pnas.0906412106

Genome sequence of a proteolytic (Group I) Clostridium botulinum strain Hall A and comparative analysis of the clostridial genomes
journal, June 2007

  • Sebaihia, M.; Peck, M. W.; Minton, N. P.
  • Genome Research, Vol. 17, Issue 7
  • DOI: 10.1101/gr.6282807

Targeted A-to-G base editing of chloroplast DNA in plants
journal, December 2022


Efficient DNA Fingerprinting of Clostridium botulinum Types A, B, E, and F by Amplified Fragment Length Polymorphism Analysis
journal, March 2005


Presence of Clostridium botulinum spores in Matricaria chamomilla (chamomile) and its relationship with infant botulism
journal, February 2008


progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement
journal, June 2010


CXCR4 signaling directs Igk recombination and the molecular mechanisms of late B lymphopoiesis
journal, September 2019

  • Mandal, Malay; Okoreeh, Michael K.; Kennedy, Domenick E.
  • Nature Immunology, Vol. 20, Issue 10
  • DOI: 10.1038/s41590-019-0468-0

Clostridium botulinum Strain Af84 Contains Three Neurotoxin Gene Clusters: Bont/A2, bont/F4 and bont/F5
journal, April 2013


Study of the presence of the spores of Clostridium botulinum in honey in Brazil
journal, July 1999


How Many Bootstrap Replicates Are Necessary?
journal, March 2010

  • Pattengale, Nicholas D.; Alipour, Masoud; Bininda-Emonds, Olaf R. P.
  • Journal of Computational Biology, Vol. 17, Issue 3
  • DOI: 10.1089/cmb.2009.0179

phangorn: phylogenetic analysis in R
journal, December 2010


BayesHammer: Bayesian clustering for error correction in single-cell sequencing
text, January 2012


A Likelihood Approach to Estimating Phylogeny from Discrete Morphological Character Data
journal, November 2001


A Rapid Bootstrap Algorithm for the RAxML Web Servers
journal, October 2008

  • Stamatakis, Alexandros; Hoover, Paul; Rougemont, Jacques
  • Systematic Biology, Vol. 57, Issue 5
  • DOI: 10.1080/10635150802429642

Implications of Genome-Based Discrimination between Clostridium botulinum Group I and Clostridium sporogenes Strains for Bacterial Taxonomy
journal, June 2015

  • Weigand, Michael R.; Pena-Gonzalez, Angela; Shirey, Timothy B.
  • Applied and Environmental Microbiology, Vol. 81, Issue 16
  • DOI: 10.1128/AEM.01159-15

Using Whole Genome Analysis to Examine Recombination across Diverse Sequence Types of Staphylococcus aureus
journal, July 2015


Whole-Genome Single-Nucleotide-Polymorphism Analysis for Discrimination of Clostridium botulinum Group I Strains
journal, January 2014

  • Gonzalez-Escalona, Narjol; Timme, Ruth; Raphael, Brian H.
  • Applied and Environmental Microbiology, Vol. 80, Issue 7
  • DOI: 10.1128/AEM.03934-13

Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Mutations in virus-derived small RNAs
journal, June 2020


QUAST: quality assessment tool for genome assemblies
journal, February 2013


Isolation and Functional Characterization of the Novel Clostridium botulinum Neurotoxin A8 Subtype
journal, February 2015


Two Novel Toxin Variants Revealed by Whole-Genome Sequencing of 175 Clostridium botulinum Type E Strains
journal, August 2014

  • Weedmark, K. A.; Lambert, D. L.; Mabon, P.
  • Applied and Environmental Microbiology, Vol. 80, Issue 20
  • DOI: 10.1128/AEM.01573-14

Improving draft assemblies by iterative mapping and assembly of short reads to eliminate gaps
journal, January 2010


BLAT---The BLAST-Like Alignment Tool
journal, March 2002


Analysis of the genetic distribution among members of Clostridium botulinum group I using a novel multilocus sequence typing (MLST) assay
journal, January 2014


Functional Characterization of Botulinum Neurotoxin Serotype H as a Hybrid of Known Serotypes F and A (BoNT F/A)
journal, March 2015

  • Kalb, Suzanne R.; Baudys, Jakub; Raphael, Brian H.
  • Analytical Chemistry, Vol. 87, Issue 7
  • DOI: 10.1021/ac504716v

Past and future species definitions for Bacteria and Archaea
journal, June 2015


Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014


Clostridium botulinum Type F: Isolation from Venison Jerky
journal, January 1972


Ancient genomes reveal social and genetic structure of Late Neolithic Switzerland
journal, April 2020

  • Furtwängler, Anja; Rohrlach, A. B.; Lamnidis, Thiseas C.
  • Nature Communications, Vol. 11, Issue 1
  • DOI: 10.1038/s41467-020-15560-x

Molecular Epidemiology of Infant Botulism in California and Elsewhere, 1976–2010
journal, June 2014

  • Dabritz, Haydee A.; Hill, Karen K.; Barash, Jason R.
  • The Journal of Infectious Diseases, Vol. 210, Issue 11
  • DOI: 10.1093/infdis/jiu331

Mosaic structures of neurotoxins produced from Clostridium botulinum types C and D organisms
journal, June 1996

  • Moriishi, Kohji; Koura, Minako; Abe, Norio
  • Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression, Vol. 1307, Issue 2
  • DOI: 10.1016/0167-4781(96)00006-1

Prevalence of Clostridium botulinum type E in Finnish fish and fishery products
journal, June 1998


Impact of recombination on bacterial evolution
journal, July 2010


A framework for variation discovery and genotyping using next-generation DNA sequencing data
journal, April 2011

  • DePristo, Mark A.; Banks, Eric; Poplin, Ryan
  • Nature Genetics, Vol. 43, Issue 5
  • DOI: 10.1038/ng.806

Distribution of Botulinum Toxin-Producing Clostridia in Soils of Argentina
journal, July 2005

  • Lúquez, Carolina; Bianco, María I.; de Jong, Laura I. T.
  • Applied and Environmental Microbiology, Vol. 71, Issue 7
  • DOI: 10.1128/aem.71.7.4137-4139.2005

RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


Prokka: rapid prokaryotic genome annotation
journal, March 2014


Clostridium botulinum Type F: Isolation from Venison Jerky
journal, August 1972


QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

Horizontal gene transfer of toxin genes in Clostridium botulinum: Involvement of mobile elements and plasmids
journal, September 2011


Genomic and physiological variability within Group II (non-proteolytic) Clostridium botulinum
journal, January 2013


Distribution of Clostridium botulinum Type E Strains in Nunavik, Northern Quebec, Canada
journal, November 2012

  • Leclair, Daniel; Farber, Jeffrey M.; Doidge, Bill
  • Applied and Environmental Microbiology, Vol. 79, Issue 2
  • DOI: 10.1128/AEM.05999-11

PATRIC, the bacterial bioinformatics database and analysis resource
journal, November 2013

  • Wattam, Alice R.; Abraham, David; Dalay, Oral
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1099

MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

Mosaic structures of neurotoxins produced from Clostridium botulinum types C and D organisms
journal, June 1996

  • Moriishi, Kohji; Koura, Minako; Abe, Norio
  • Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression, Vol. 1307, Issue 2
  • DOI: 10.1016/0167-4781(96)00006-1

Genetic Diversity among Botulinum Neurotoxin-Producing Clostridial Strains
journal, November 2006

  • Hill, K. K.; Smith, T. J.; Helma, C. H.
  • Journal of Bacteriology, Vol. 189, Issue 3
  • DOI: 10.1128/JB.01180-06

Analysis of the genetic distribution among members of Clostridium botulinum group I using a novel multilocus sequence typing (MLST) assay
journal, January 2014


BayesHammer: Bayesian clustering for error correction in single-cell sequencing
journal, January 2013

  • Nikolenko, Sergey I.; Korobeynikov, Anton I.; Alekseyev, Max A.
  • BMC Genomics, Vol. 14, Issue Suppl 1
  • DOI: 10.1186/1471-2164-14-S1-S7

Versatile and open software for comparing large genomes
journal, January 2004

  • Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L.
  • Genome Biology, Vol. 5, Issue 2, R12
  • DOI: 10.1186/gb-2004-5-2-r12

A novel algorithm and web-based tool for comparing two alternative phylogenetic trees
journal, October 2005


Phylogeny and taxonomy of the food-borne pathogen Clostridium botulinum and its neurotoxins
journal, January 1998


Draft Genome Sequence of Comamonas aquatilis Strain LK (= CSUR P6418 = CECT 9772), Isolated from the Planarian Schmidtea mediterranea
journal, February 2021

  • Kangale, Luis Johnson; Levasseur, Anthony; Raoult, Didier
  • Microbiology Resource Announcements, Vol. 10, Issue 5
  • DOI: 10.1128/mra.00297-20

Impact of recombination on bacterial evolution
journal, July 2010


Using Whole Genome Analysis to Examine Recombination across Diverse Sequence Types of Staphylococcus aureus
journal, July 2015


Past and future species definitions for Bacteria and Archaea
journal, June 2015


Genomic Epidemiology of Clostridium botulinum Isolates from Temporally Related Cases of Infant Botulism in New South Wales, Australia
journal, June 2015

  • McCallum, Nadine; Gray, Timothy J.; Wang, Qinning
  • Journal of Clinical Microbiology, Vol. 53, Issue 9
  • DOI: 10.1128/jcm.00143-15

Molecular Epidemiology of Infant Botulism in California and Elsewhere, 1976–2010
journal, June 2014

  • Dabritz, Haydee A.; Hill, Karen K.; Barash, Jason R.
  • The Journal of Infectious Diseases, Vol. 210, Issue 11
  • DOI: 10.1093/infdis/jiu331

Analysis of Neurotoxin Cluster Genes in Clostridium botulinum Strains Producing Botulinum Neurotoxin Serotype A Subtypes
journal, March 2008

  • Jacobson, Mark J.; Lin, Guangyun; Raphael, Brian
  • Applied and Environmental Microbiology, Vol. 74, Issue 9
  • DOI: 10.1128/AEM.02828-07

Phylogenetic analysis of Clostridium botulinum type A by multi-locus sequence typing
journal, August 2008


The Northern Arizona SNP Pipeline (NASP): accurate, flexible, and rapid identification of SNPs in WGS datasets
posted_content, January 2016

  • Sahl, Jason W.; Lemmer, Darrin; Travis, Jason
  • Microbial Genomics
  • DOI: 10.1101/037267

Genomic Analysis of Clostridium botulinum Group II by Pulsed-Field Gel Electrophoresis
journal, February 1998

  • Hielm, Sebastian; Björkroth, Johanna; Hyytiä, Eija
  • Applied and Environmental Microbiology, Vol. 64, Issue 2
  • DOI: 10.1128/aem.64.2.703-708.1998

Search and clustering orders of magnitude faster than BLAST
journal, August 2010


The large-scale blast score ratio (LS-BSR) pipeline: a method to rapidly compare genetic content between bacterial genomes
journal, January 2014

  • Sahl, Jason W.; Caporaso, J. Gregory; Rasko, David A.
  • PeerJ, Vol. 2
  • DOI: 10.7717/peerj.332

BLAT---The BLAST-Like Alignment Tool
journal, March 2002


Molecular Characterization of a Novel Botulinum Neurotoxin Type H Gene
journal, October 2013

  • Dover, Nir; Barash, Jason R.; Hill, Karen K.
  • The Journal of Infectious Diseases, Vol. 209, Issue 2
  • DOI: 10.1093/infdis/jit450

Accurate and universal delineation of prokaryotic species
journal, July 2013

  • Mende, Daniel R.; Sunagawa, Shinichi; Zeller, Georg
  • Nature Methods, Vol. 10, Issue 9
  • DOI: 10.1038/nmeth.2575

PATRIC, the bacterial bioinformatics database and analysis resource
journal, November 2013

  • Wattam, Alice R.; Abraham, David; Dalay, Oral
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1099

Historical and current perspectives on Clostridium botulinum diversity
journal, May 2015


Comparative Genomic Hybridization Analysis of Two Predominant Nordic Group I (Proteolytic) Clostridium botulinum Type B Clusters
journal, March 2009

  • Lindström, Miia; Hinderink, Katja; Somervuo, Panu
  • Applied and Environmental Microbiology, Vol. 75, Issue 9
  • DOI: 10.1128/aem.02557-08

Clostridium botulinum Strain Af84 Contains Three Neurotoxin Gene Clusters: Bont/A2, bont/F4 and bont/F5
journal, April 2013


Analysis of a unique Clostridium botulinum strain from the Southern hemisphere producing a novel type E botulinum neurotoxin subtype
journal, January 2012

  • Raphael, Brian H.; Lautenschlager, Matthew; Kalb, Suzanne R.
  • BMC Microbiology, Vol. 12, Issue 1
  • DOI: 10.1186/1471-2180-12-245

The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
journal, July 2010


Horizontal gene transfer of toxin genes in Clostridium botulinum: Involvement of mobile elements and plasmids
journal, September 2011


BIGSdb: Scalable analysis of bacterial genome variation at the population level
journal, December 2010


Clostridium botulinum Group II Isolate Phylogenomic Profiling Using Whole-Genome Sequence Data
journal, June 2015

  • Weedmark, K. A.; Mabon, P.; Hayden, K. L.
  • Applied and Environmental Microbiology, Vol. 81, Issue 17
  • DOI: 10.1128/aem.01155-15

Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement
journal, November 2014


Clostridium botulinum Strains Producing BoNT/F4 or BoNT/F5
journal, March 2014

  • Raphael, Brian H.; Bradshaw, Marite; Kalb, Suzanne R.
  • Applied and Environmental Microbiology, Vol. 80, Issue 10
  • DOI: 10.1128/AEM.00284-14

Draft Genome Sequence of Medusavirus Stheno, Isolated from the Tatakai River of Uji, Japan
journal, January 2021

  • Yoshida, Koki; Zhang, Ruixuan; Garcia, Kimberly G.
  • Microbiology Resource Announcements, Vol. 10, Issue 1
  • DOI: 10.1128/mra.01323-20

Improving draft assemblies by iterative mapping and assembly of short reads to eliminate gaps
journal, January 2010


Isolation of Clostridium botulinum from Honey
journal, February 1979


Works referencing / citing this record:

An Integrative Approach to Computational Modelling of the Gene Regulatory Network Controlling Clostridium botulinum Type A1 Toxin Production
journal, November 2016


Historical Perspectives and Guidelines for Botulinum Neurotoxin Subtype Nomenclature
journal, January 2017


Historical Perspectives and Guidelines for Botulinum Neurotoxin Subtype Nomenclature
journal, January 2017


Diversity of Group I and II Clostridium botulinum Strains from France Including Recently Identified Subtypes
journal, April 2016

  • Mazuet, Christelle; Legeay, Christine; Sautereau, Jean
  • Genome Biology and Evolution, Vol. 8, Issue 6
  • DOI: 10.1093/gbe/evw101

Differentiating Botulinum Neurotoxin-Producing Clostridia with a Simple, Multiplex PCR Assay
journal, July 2017

  • Williamson, Charles H. D.; Vazquez, Adam J.; Hill, Karen
  • Applied and Environmental Microbiology, Vol. 83, Issue 18
  • DOI: 10.1128/aem.00806-17

Diversity of the Germination Apparatus in Clostridium botulinum Groups I, II, III, and IV
journal, October 2016

  • Brunt, Jason; van Vliet, Arnoud H. M.; van den Bos, Fédor
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.01702

Optimization of SNAP-25 and VAMP-2 Cleavage by Botulinum Neurotoxin Serotypes A–F Employing Taguchi Design-of-Experiments
journal, October 2019


Optimization of SNAP-25 and VAMP-2 Cleavage by Botulinum Neurotoxin Serotypes A–F Employing Taguchi Design-of-Experiments
journal, October 2019


Botulinum neurotoxin–encoding plasmids can be conjugatively transferred to diverse clostridial strains
journal, February 2018


Genomic insights into the evolution and ecology of botulinum neurotoxins
journal, April 2018

  • Mansfield, Michael J.; Doxey, Andrew C.
  • Pathogens and Disease, Vol. 76, Issue 4
  • DOI: 10.1093/femspd/fty040

Reoccurrence of botulinum neurotoxin subtype A3 inducing food-borne botulism, Slovakia, 2015
journal, August 2017


Genetic Characterization of the Exceptionally High Heat Resistance of the Non-toxic Surrogate Clostridium sporogenes PA 3679
journal, April 2017


Novel Botulinum Neurotoxins: Exploring Underneath the Iceberg Tip
journal, May 2018


Botulinum Neurotoxin Detection Methods for Public Health Response and Surveillance
journal, June 2018

  • Thirunavukkarasu, Nagarajan; Johnson, Eric; Pillai, Segaran
  • Frontiers in Bioengineering and Biotechnology, Vol. 6
  • DOI: 10.3389/fbioe.2018.00080

The role of the single interchains disulfide bond in tetanus and botulinum neurotoxins and the development of antitetanus and antibotulism drugs
journal, May 2019

  • Rossetto, Ornella; Pirazzini, Marco; Lista, Florigio
  • Cellular Microbiology, Vol. 21, Issue 11
  • DOI: 10.1111/cmi.13037

Diversity of Group I and II Clostridium botulinum Strains from France Including Recently Identified Subtypes
journal, April 2016

  • Mazuet, Christelle; Legeay, Christine; Sautereau, Jean
  • Genome Biology and Evolution, Vol. 8, Issue 6
  • DOI: 10.1093/gbe/evw101