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

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

doi:10.1186/s12864-016-2502-z

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

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

DOI:https://doi.org/10.1186/s12864-016-2502-z· OSTI ID:1626797

Williamson, Charles H. D. ^[1]; Sahl, Jason W. ^[2]; Smith, Theresa J. ^[3]; Xie, Gary ^[4]; Foley, Brian T. ^[5]; Smith, Leonard A. ^[6]; Fernández, Rafael A. ^[7]; Lindström, Miia ^[8]; Korkeala, Hannu ^[8]; Keim, Paul ^[2]; Foster, Jeffrey ^[2]; Hill, Karen ^[4]

Northern Arizona Univ., Flagstaff, AZ (United States). Center for Microbial Genetics and Genomics; DOE/OSTI
Northern Arizona Univ., Flagstaff, AZ (United States). Center for Microbial Genetics and Genomics
US Army Medical Research Inst. of Infectious Diseases, Fort Detrick, MD (United States)
Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Bioscience Div.
Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Div.
US Army Medical Research Inst of Infecgious Diseases, Fort Detrick, MD (United States). Medical Countermeasures Technology, US Army Medical Research and Material Command
Área Microbiología, Departamento de Patología, Facultad de Ciencias Médicas, Universidad Nacional de Cuyo, Centro Universitario, Mendoza (Argentina)
Univ. of Helsinki (Finland). Dept. of Food Hygiene and Environmental Health

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.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: U.S. Department of Homeland Security; USDOE

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1626797

Journal Information:: BMC Genomics, Journal Name: BMC Genomics Journal Issue: 1 Vol. 17; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Comparison of Clostridium botulinum genomes shows the absence of cold shock protein coding genes in type E neurotoxin producing strains Söderholm, Henna; Jaakkola, Kaisa; Somervuo, Panu The Botulinum J., Vol. 2, Issue 3/4 https://doi.org/10.1504/TBJ.2013.055662	journal	January 2013
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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
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An Integrative Approach to Computational Modelling of the Gene Regulatory Network Controlling Clostridium botulinum Type A1 Toxin Production Ihekwaba, Adaoha E. C.; Mura, Ivan; Walshaw, John PLOS Computational Biology, Vol. 12, Issue 11 https://doi.org/10.1371/journal.pcbi.1005205	journal	November 2016
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Table 1(p. 6)

Table 1 (Continued)(p. 7)

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59 BASIC BIOLOGICAL SCIENCES
Clostridium botulinum
Biotechnology & Applied Microbiology
Botulinum neurotoxin
Comparative
Genetics & Heredity
Whole genome sequence

Additional file 2: Table S2. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/M9.FIGSHARE.C.3630344_D6 The current record is supplemented by this dataset	dataset	January 2016
Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344 The current record is supplemented by this collection	collection	January 2016
Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344.v1 The current record is supplemented by this collection	collection	January 2016
Additional file 3: Table S3. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d1 The current record is supplemented by this dataset	dataset	January 2016
Additional file 3: Table S3. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d1.v1 The current record is supplemented by this dataset	dataset	January 2016
Additional file 6: Figure S3. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d2 The current record is supplemented by this text	text	January 2016
Additional file 6: Figure S3. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d2.v1 The current record is supplemented by this text	text	January 2016
Additional file 9: Figure S6. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d3 The current record is supplemented by this text	text	January 2016
Additional file 9: Figure S6. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d3.v1 The current record is supplemented by this text	text	January 2016
Additional file 5: Figure S2. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d4 The current record is supplemented by this text	text	January 2016
Additional file 5: Figure S2. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d4.v1 The current record is supplemented by this text	text	January 2016
Additional file 8: Figure S5. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d5 The current record is supplemented by this text	text	January 2016
Additional file 8: Figure S5. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d5.v1 The current record is supplemented by this text	text	January 2016
Additional file 2: Table S2. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d6.v1 The current record is supplemented by this dataset	dataset	January 2016
Additional file 7: Figure S4. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d7 The current record is supplemented by this text	text	January 2016
Additional file 7: Figure S4. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d7.v1 The current record is supplemented by this text	text	January 2016
Additional file 4: Figure S1. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d8 The current record is supplemented by this text	text	January 2016
Additional file 4: Figure S1. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d8.v1 The current record is supplemented by this text	text	January 2016
Additional file 1: Table S1. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d9 The current record is supplemented by this dataset	dataset	January 2016
Additional file 1: Table S1. of Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles; Sahl, Jason; Smith, Theresa https://doi.org/10.6084/m9.figshare.c.3630344_d9.v1 The current record is supplemented by this dataset	dataset	January 2016

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

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