Genetic diversity within the botulinum neurotoxin-producing bacteria and their neurotoxins

Hill, Karen Koons; Xie, Gary; Foley, Brian T.; Smith, Theresa J.

doi:10.1016/j.toxicon.2015.09.011

Title: Genetic diversity within the botulinum neurotoxin-producing bacteria and their neurotoxins

Journal Article · Fri Sep 11 00:00:00 EDT 2015 · Toxicon

DOI:https://doi.org/10.1016/j.toxicon.2015.09.011· OSTI ID:1457238

Hill, Karen Koons ^[1];

^[1];

^[1]; Smith, Theresa J. ^[2]

Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
US Army Medical Research Inst. of Infectious Diseases (USAMRIID), Fort Detrick, MD (United States). Molecular and Translational Sciences Division

The recent availability of multiple Clostridium botulinum genomic sequences has initiated a new genomics era that strengthens our understanding of the bacterial species that produce botulinum neurotoxins (BoNTs). Analysis of the genomes has reinforced the historical Group I–VI designations and provided evidence that the bont genes can be located within the chromosome, phage or plasmids. The sequences provide the opportunity to examine closely the variation among the toxin genes, the composition and organization of the toxin complex, the regions flanking the toxin complex and the location of the toxin within different bacterial strains. These comparisons provide evidence of horizontal gene transfer and site-specific insertion and recombination events that have contributed to the variation observed among the neurotoxins. In this work, examples that have contributed to the variation observed in serotypes A-H strains are presented to illustrate the mechanisms that have contributed to their variation.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); National Institutes of Health (NIH)

Grant/Contract Number:: AC52-06NA25396; U01 AI056493

OSTI ID:: 1457238

Report Number(s):: LA-UR-15-23061

Journal Information:: Toxicon, Vol. 107, Issue PA; ISSN 0041-0101

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 53 works

Citation information provided by
Web of Science

References (23)

Three Classes of Plasmid (47–63 kb) Carry the Type B Neurotoxin Gene Cluster of Group II Clostridium botulinum Carter, Andrew T.; Austin, John W.; Weedmark, Kelly A. Genome Biology and Evolution, Vol. 6, Issue 8 https://doi.org/10.1093/gbe/evu164	journal	July 2014
Complete Genome Sequence of the Proteolytic Clostridium botulinum Type A5 (B3′) Strain H04402 065 Carter, Andrew T.; Pearson, Bruce M.; Crossman, Lisa C. Journal of Bacteriology, Vol. 193, Issue 9 https://doi.org/10.1128/JB.00072-11	journal	May 2011
The Type F6 Neurotoxin Gene Cluster Locus of Group II Clostridium botulinum Has Evolved by Successive Disruption of Two Different Ancestral Precursors Carter, Andrew T.; Stringer, Sandra C.; Webb, Martin D. Genome Biology and Evolution, Vol. 5, Issue 5 https://doi.org/10.1093/gbe/evt068	journal	May 2013
Quantitative Real-Time Reverse Transcription-PCR Analysis Reveals Stable and Prolonged Neurotoxin Cluster Gene Activity in a Clostridium botulinum Type E Strain at Refrigeration Temperature Chen, Ying; Korkeala, Hannu; Lindén, Jere Applied and Environmental Microbiology, Vol. 74, Issue 19 https://doi.org/10.1128/AEM.00469-08	journal	October 2008
Regulation of toxin synthesis in Clostridium botulinum and Clostridium tetani Connan, Chloé; Denève, Cécile; Mazuet, Christelle Toxicon, Vol. 75 https://doi.org/10.1016/j.toxicon.2013.06.001	journal	December 2013
Arrangement of the Clostridium baratii F7 Toxin Gene Cluster with Identification of a σ Factor That Recognizes the Botulinum Toxin Gene Cluster Promoters Dover, Nir; Barash, Jason R.; Burke, Julianne N. PLoS ONE, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pone.0097983	journal	May 2014
Clostridium botulinum Strain Af84 Contains Three Neurotoxin Gene Clusters: Bont/A2, bont/F4 and bont/F5 Dover, Nir; Barash, Jason R.; Hill, Karen K. PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061205	journal	April 2013
Molecular Characterization of a Novel Botulinum Neurotoxin Type H Gene Dover, Nir; Barash, Jason R.; Hill, Karen K. The Journal of Infectious Diseases, Vol. 209, Issue 2 https://doi.org/10.1093/infdis/jit450	journal	October 2013
Organization and Phylogenetic Interrelationships of Genes Encoding Components of the Botulinum Toxin Complex in Proteolytic Clostridium botulinum Types A, B, and F: Evidence of Chimeric Sequences in the Gene Encoding the Nontoxic Nonhemagglutinin Component East, A. K.; Bhandari, M.; Stacey, J. M. International Journal of Systematic Bacteriology, Vol. 46, Issue 4 https://doi.org/10.1099/00207713-46-4-1105	journal	October 1996
Evidence that Plasmid-Borne Botulinum Neurotoxin Type B Genes Are Widespread among Clostridium botulinum Serotype B Strains Franciosa, Giovanna; Maugliani, Antonella; Scalfaro, Concetta PLoS ONE, Vol. 4, Issue 3 https://doi.org/10.1371/journal.pone.0004829	journal	March 2009
Draft Genome Sequence of Bivalent Clostridium botulinum Strain IBCA10-7060, Encoding Botulinum Neurotoxin B and a New FA Mosaic Type Gonzalez-Escalona, N.; Thirunavukkarasu, N.; Singh, A. Genome Announcements, Vol. 2, Issue 6 https://doi.org/10.1128/genomeA.01275-14	journal	November 2014
Organization of the botulinum neurotoxin C1 gene and its associated non-toxic protein genes in Clostridium botulinum C468 Hauser, Daniel; Eklund, Mel W.; Boquet, Patrice Molecular and General Genetics MGG, Vol. 243, Issue 6 https://doi.org/10.1007/BF00279572	journal	November 1994
Genetic Diversity among Botulinum Neurotoxin-Producing Clostridial Strains Hill, K. K.; Smith, T. J.; Helma, C. H. Journal of Bacteriology, Vol. 189, Issue 3 https://doi.org/10.1128/JB.01180-06	journal	November 2006
Recombination and insertion events involving the botulinum neurotoxin complex genes in Clostridium botulinum types A, B, E and F and Clostridium butyricumtype E strains Hill, Karen K.; Xie, Gary; Foley, Brian T. BMC Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1741-7007-7-66	journal	October 2009
Functional Characterization of Botulinum Neurotoxin Serotype H as a Hybrid of Known Serotypes F and A (BoNT F/A) Kalb, Suzanne R.; Baudys, Jakub; Raphael, Brian H. Analytical Chemistry, Vol. 87, Issue 7 https://doi.org/10.1021/ac504716v	journal	March 2015
Isolation and Functional Characterization of the Novel Clostridium botulinum Neurotoxin A8 Subtype Kull, Skadi; Schulz, K. Melanie; Strotmeier, Jasmin Weisemann née PLOS ONE, Vol. 10, Issue 2 https://doi.org/10.1371/journal.pone.0116381	journal	February 2015
Analysis of a unique Clostridium botulinum strain from the Southern hemisphere producing a novel type E botulinum neurotoxin subtype Raphael, Brian H.; Lautenschlager, Matthew; Kalb, Suzanne R. BMC Microbiology, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2180-12-245	journal	January 2012
The genome sequence of Clostridium botulinum type C neurotoxin-converting phage and the molecular mechanisms of unstable lysogeny Sakaguchi, Y.; Hayashi, T.; Kurokawa, K. Proceedings of the National Academy of Sciences, Vol. 102, Issue 48 https://doi.org/10.1073/pnas.0505503102	journal	November 2005
Genomic sequences of six botulinum neurotoxin-producing strains representing three clostridial species illustrate the mobility and diversity of botulinum neurotoxin genes Smith, Theresa J.; Hill, Karen K.; Xie, Gary Infection, Genetics and Evolution, Vol. 30 https://doi.org/10.1016/j.meegid.2014.12.002	journal	March 2015
Molecular Characterization of Clostridium botulinum Isolates from Foodborne Outbreaks in Thailand, 2010 Wangroongsarb, Piyada; Kohda, Tomoko; Jittaprasartsin, Chutima PLoS ONE, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pone.0077792	journal	January 2014
Protection with recombinant Clostridium botulinum C1 and D binding domain subunit (Hc) vaccines against C and D neurotoxins Webb, Robert P.; Smith, Theresa J.; Wright, Patrick M. Vaccine, Vol. 25, Issue 21 https://doi.org/10.1016/j.vaccine.2007.02.081	journal	May 2007
Two Novel Toxin Variants Revealed by Whole-Genome Sequencing of 175 Clostridium botulinum Type E Strains Weedmark, K. A.; Lambert, D. L.; Mabon, P. Applied and Environmental Microbiology, Vol. 80, Issue 20 https://doi.org/10.1128/AEM.01573-14	journal	August 2014
Plasmid-Borne Type E Neurotoxin Gene Clusters in Clostridium botulinum Strains Zhang, Zhen; Hintsa, Hannamari; Chen, Ying Applied and Environmental Microbiology, Vol. 79, Issue 12 https://doi.org/10.1128/AEM.00080-13	journal	April 2013

Cited By (24)

A Rapid, Sensitive, and Portable Biosensor Assay for the Detection of Botulinum Neurotoxin Serotype A in Complex Food Matrices Tam, Christina; Flannery, Andrew; Cheng, Luisa Toxins, Vol. 10, Issue 11 https://doi.org/10.3390/toxins10110476	journal	November 2018
Engineered botulinum neurotoxin B with improved efficacy for targeting human receptors Tao, Liang; Peng, Lisheng; Berntsson, Ronnie P. -A. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00064-y	journal	July 2017
PCR-based molecular diagnosis of botulism (types C and D) outbreaks in aquatic birds Chellapandi, Paulchamy; Prisilla, Arockiasamy Annals of Microbiology, Vol. 68, Issue 12 https://doi.org/10.1007/s13213-018-1390-7	journal	October 2018
Identification of a novel botulinum neurotoxin gene cluster in Enterococcus Brunt, Jason; Carter, Andrew T.; Stringer, Sandra C. FEBS Letters, Vol. 592, Issue 3 https://doi.org/10.1002/1873-3468.12969	journal	January 2018
Structural basis for the unique ganglioside and cell membrane recognition mechanism of botulinum neurotoxin DC Zhang, Sicai; Berntsson, Ronnie P. -A.; Tepp, William H. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01534-z	journal	November 2017
Critical Analysis of Neuronal Cell and the Mouse Bioassay for Detection of Botulinum Neurotoxins Pellett, Sabine; Tepp, William H.; Johnson, Eric A. Toxins, Vol. 11, Issue 12 https://doi.org/10.3390/toxins11120713	journal	December 2019
Engineering of Botulinum Neurotoxins for Biomedical Applications Webb, Robert Toxins, Vol. 10, Issue 6 https://doi.org/10.3390/toxins10060231	journal	June 2018
The Light Chain Defines the Duration of Action of Botulinum Toxin Serotype A Subtypes Pellett, Sabine; Bradshaw, Marite; Tepp, William H. mBio, Vol. 9, Issue 2 https://doi.org/10.1128/mbio.00089-18	journal	March 2018
Why Are Botulinum Neurotoxin-Producing Bacteria So Diverse and Botulinum Neurotoxins So Toxic? Poulain, Bernard; Popoff, Michel Toxins, Vol. 11, Issue 1 https://doi.org/10.3390/toxins11010034	journal	January 2019
The Novel Clostridial Neurotoxin Produced by Strain IBCA10-7060 Is Immunologically Equivalent to BoNT/HA Fan, Yongfeng; Barash, Jason R.; Conrad, Fraser Toxins, Vol. 12, Issue 1 https://doi.org/10.3390/toxins12010009	journal	December 2019
Identification and characterization of a novel botulinum neurotoxin Zhang, Sicai; Masuyer, Geoffrey; Zhang, Jie Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14130	journal	August 2017
Historical Perspectives and Guidelines for Botulinum Neurotoxin Subtype Nomenclature Peck, Michael; Smith, Theresa; Anniballi, Fabrizio Toxins, Vol. 9, Issue 1 https://doi.org/10.3390/toxins9010038	journal	January 2017
Microbiota Signaling Pathways that Influence Neurologic Disease Cox, Laura M.; Weiner, Howard L. Neurotherapeutics, Vol. 15, Issue 1 https://doi.org/10.1007/s13311-017-0598-8	journal	January 2018
The orphan germinant receptor protein GerXAO (but not GerX3b) is essential for L-alanine induced germination in Clostridium botulinum Group II Brunt, Jason; Carter, Andrew T.; Pye, Hannah V. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-25411-x	journal	May 2018
In silico mutagenesis: decreasing the immunogenicity of botulinum toxin type A Evander Emeltan Tjoa, Stanley; Maria Vianney, Yoanes; Emantoko Dwi Putra, Sulistyo Journal of Biomolecular Structure and Dynamics, Vol. 37, Issue 18 https://doi.org/10.1080/07391102.2018.1559100	journal	January 2019
Diversity of Group I and II Clostridium botulinum Strains from France Including Recently Identified Subtypes Mazuet, Christelle; Legeay, Christine; Sautereau, Jean Genome Biology and Evolution, Vol. 8, Issue 6 https://doi.org/10.1093/gbe/evw101	journal	April 2016
In silico mutagenesis: decreasing the immunogenicity of botulinum toxin type A Tjoa, Stanley Evander Emeltan; Vianney, Yoanes Maria; Putra, Sulistyo Emantoko Dwi Taylor & Francis https://doi.org/10.6084/m9.figshare.7593890.v1	text	January 2019
A Rapid, Sensitive, and Portable Biosensor Assay for the Detection of Botulinum Neurotoxin Serotype A in Complex Food Matrices Tam, Christina C.; Flannery, Andrew R.; Cheng, Luisa W. Preprints.org https://doi.org/10.20944/preprints201808.0390.v1	posted_content	August 2018
In silico mutagenesis: decreasing the immunogenicity of botulinum toxin type A Tjoa, Stanley Evander Emeltan; Vianney, Yoanes Maria; Putra, Sulistyo Emantoko Dwi Taylor & Francis https://doi.org/10.6084/m9.figshare.7593890	text	January 2019
The pattern of growth observed forClostridium botulinumtype A1 strain ATCC 19397 is influenced by nutritional status and quorum sensing: a modelling perspective Ihekwaba, Adaoha E. C.; Mura, Ivan; Peck, Michael W. Pathogens and Disease, Vol. 73, Issue 9 https://doi.org/10.1093/femspd/ftv084	journal	October 2015
Characterization of a membrane binding loop leads to engineering botulinum neurotoxin B with improved therapeutic efficacy Yin, Linxiang; Masuyer, Geoffrey; Zhang, Sicai PLOS Biology, Vol. 18, Issue 3 https://doi.org/10.1371/journal.pbio.3000618	journal	March 2020
Diversity of the Germination Apparatus in Clostridium botulinum Groups I, II, III, and IV Brunt, Jason; van Vliet, Arnoud H. M.; van den Bos, Fédor Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01702	journal	October 2016
Probiotic Microorganisms Inhibit Epithelial Cell Internalization of Botulinum Neurotoxin Serotype A Lam, Tina; Tam, Christina; Stanker, Larry Toxins, Vol. 8, Issue 12 https://doi.org/10.3390/toxins8120377	journal	December 2016
Vaccines against Botulism Sundeen, Grace; Barbieri, Joseph Toxins, Vol. 9, Issue 9 https://doi.org/10.3390/toxins9090268	journal	September 2017

Similar Records

The Distinctive Evolution of orfX Clostridium parabotulinum Strains and Their Botulinum Neurotoxin Type A and F Gene Clusters Is Influenced by Environmental Factors and Gene Interactions via Mobile Genetic Elements

Journal Article · Fri Feb 26 00:00:00 EST 2021 · Frontiers in Microbiology · OSTI ID:1457238

Smith, Theresa J.; Williamson, Charles D.; Hill, Karen K.; +8 more

Genetic Diversity Among Botulinum Neurotoxin Producing Clostridial Strains

Journal Article · Thu Jul 06 00:00:00 EDT 2006 · Journal of Bacteriology · OSTI ID:1457238

Hill, K K; Smith, T J; Helma, C H; +9 more

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

Journal Article · Thu Mar 03 00:00:00 EST 2016 · BMC Genomics · OSTI ID:1457238

Williamson, Charles H. D.; Sahl, Jason W.; Smith, Theresa J.; +9 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
genetic diversity
botulinum neurotoxin
Clostridium botulinum

Title: Genetic diversity within the botulinum neurotoxin-producing bacteria and their neurotoxins

Citation Formats

References (23)

Cited By (24)

Similar Records

Related Subjects