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

Smith, Theresa J.; Williamson, Charles D.; Hill, Karen K.; Johnson, Shannon L.; Xie, Gary; Anniballi, Fabrizio; Auricchio, Bruna; Fernández, Rafael A.; Caballero, Patricia A.; Keim, Paul; Sahl, Jason W.

doi:10.3389/fmicb.2021.566908

Title: 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

DOI:https://doi.org/10.3389/fmicb.2021.566908· OSTI ID:1868218

Smith, Theresa J. ^[1]; Williamson, Charles D. ^[1]; Hill, Karen K. ^[2];

^[2];

^[2]; Anniballi, Fabrizio ^[3]; Auricchio, Bruna ^[3]; Fernández, Rafael A. ^[4]; Caballero, Patricia A. ^[4]; Keim, Paul ^[1]; Sahl, Jason W. ^[1]

Northern Arizona Univ., Flagstaff, AZ (United States)
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Istituto Superiore di Sanita, Rome (Italy)
Universidad Nacional de Cuyo, Mendoza (Argentina)

Of the seven currently known botulinum neurotoxin-producing species of Clostridium, C. parabotulinum, or C. botulinum Group I, is the species associated with the majority of human botulism cases worldwide. Phylogenetic analysis of these bacteria reveals a diverse species with multiple genomic clades. The neurotoxins they produce are also diverse, with over 20 subtypes currently represented. The existence of different bont genes within very similar genomes and of the same bont genes/gene clusters within different bacterial variants/species indicates that they have evolved independently. The neurotoxin genes are associated with one of two toxin gene cluster types containing either hemagglutinin (ha) genes or orfX genes. These genes may be located within the chromosome or extrachromosomal elements such as large plasmids. Although BoNT-producing C parabotulinum bacteria are distributed globally, they are more ubiquitous in certain specific geographic regions. Notably, northern hemisphere strains primarily contain ha gene clusters while southern hemisphere strains have a preponderance of orfX gene clusters. OrfX C. parabotulinum strains constitute a subset of this species that contain highly conserved bont gene clusters having a diverse range of bont genes. While much has been written about strains with ha gene clusters, less attention has been devoted to those with orfX gene clusters. The recent sequencing of 28 orfX C. parabotulinum strains and the availability of an additional 91 strains for analysis provides an opportunity to compare genomic relationships and identify unique toxin gene cluster characteristics and locations within this species subset in depth. The mechanisms behind the independent processes of bacteria evolution and generation of toxin diversity are explored through the examination of bacterial relationships relating to source locations and evidence of horizontal transfer of genetic material among different bacterial variants, particularly concerning bont gene clusters. Analysis of the content and locations of the bont gene clusters offers insights into common mechanisms of genetic transfer, chromosomal integration, and development of diversity among these genes.

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

Sponsoring Organization:: U.S. Department of Homeland Security (DHS); USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: 89233218CNA000001; HSHQDC-16-C-B0013

OSTI ID:: 1868218

Report Number(s):: LA-UR-20-24104

Journal Information:: Frontiers in Microbiology, Vol. 12; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (71)

Genomic Epidemiology of Clostridium botulinum Isolates from Temporally Related Cases of Infant Botulism in New South Wales, Australia McCallum, Nadine; Gray, Timothy J.; Wang, Qinning Journal of Clinical Microbiology, Vol. 53, Issue 9 https://doi.org/10.1128/JCM.00143-15	journal	June 2015
BayesHammer: Bayesian clustering for error correction in single-cell sequencing Nikolenko, Sergey I.; Korobeynikov, Anton I.; Alekseyev, Max A. BMC Genomics, Vol. 14, Issue Suppl 1 https://doi.org/10.1186/1471-2164-14-S1-S7	journal	January 2013
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
Genetic confirmation of identities of neurotoxigenic Clostridium baratii and Clostridium butyricum implicated as agents of infant botulism. Suen, J. C.; Hatheway, C. L.; Steigerwalt, A. G. Journal of Clinical Microbiology, Vol. 26, Issue 10 https://doi.org/10.1128/JCM.26.10.2191-2192.1988	journal	January 1988
Versatile and open software for comparing large genomes Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L. Genome Biology, Vol. 5, Issue 2, R12 https://doi.org/10.1186/gb-2004-5-2-r12	journal	January 2004
Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia Williamson, Charles H. D.; Sahl, Jason W.; Smith, Theresa J. BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-2502-z	journal	March 2016
Phylogeny and taxonomy of the food-borne pathogen Clostridium botulinum and its neurotoxins Journal of Applied Microbiology, Vol. 84, Issue 1 https://doi.org/10.1046/j.1365-2672.1997.00313.x	journal	January 1998
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
Genetic Diversity among Clostridium botulinum Strains Harboring bont/A2 and bont/A3 Genes Lúquez, Carolina; Raphael, Brian H.; Joseph, Lavin A. Applied and Environmental Microbiology, Vol. 78, Issue 24 https://doi.org/10.1128/AEM.02428-12	journal	October 2012
Conjugative Botulinum Neurotoxin-Encoding Plasmids in Clostridium botulinum Marshall, Kristin M.; Bradshaw, Marite; Johnson, Eric A. PLoS ONE, Vol. 5, Issue 6 https://doi.org/10.1371/journal.pone.0011087	journal	June 2010
A New Anaerobic Bacillus and Its Relation to Botulism van Ermengem, E. Clinical Infectious Diseases, Vol. 1, Issue 4 https://doi.org/10.1093/clinids/1.4.701	journal	July 1979
Neurotoxin Gene Clusters in Clostridium botulinum Type A Strains: Sequence Comparison and Evolutionary Implications Dineen, Sean S.; Bradshaw, Marite; Johnson, Eric A. Current Microbiology, Vol. 46, Issue 5 https://doi.org/10.1007/s00284-002-3851-1	journal	May 2003
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
Phylogenetic basis for a taxonomic dissection of the genus Clostridium Stackebrandt, E.; Kramer, I.; Swiderski, J. FEMS Immunology & Medical Microbiology, Vol. 24, Issue 3 https://doi.org/10.1111/j.1574-695X.1999.tb01291.x	journal	July 1999
South African Cultures of Clostridium Botulinum and Parabotulinum. XXXVII: With a Description of CL. Botulinum Type D, N.SP. Meyer, K. F.; Gunnison, J. B. Journal of Infectious Diseases, Vol. 45, Issue 2 https://doi.org/10.1093/infdis/45.2.106	journal	August 1929
Botulinum Neurotoxin-Producing Bacteria. Isn’t It Time that We Called a Species a Species? Smith, Theresa; Williamson, Charles H. D.; Hill, Karen mBio, Vol. 9, Issue 5 https://doi.org/10.1128/mBio.01469-18	journal	September 2018
NASP: an accurate, rapid method for the identification of SNPs in WGS datasets that supports flexible input and output formats Sahl, Jason W.; Lemmer, Darrin; Travis, Jason Microbial Genomics, Vol. 2, Issue 8 https://doi.org/10.1099/mgen.0.000074	journal	August 2016
Nucleotide sequence and transcriptional analysis of the type A2 neurotoxin gene cluster in Clostridium botulinum Dineen, S. FEMS Microbiology Letters, Vol. 235, Issue 1 https://doi.org/10.1016/j.femsle.2004.04.002	journal	June 2004
Genomic characterization of Italian Clostridium botulinum group I strains Giordani, Francesco; Fillo, Silvia; Anselmo, Anna Infection, Genetics and Evolution, Vol. 36 https://doi.org/10.1016/j.meegid.2015.08.042	journal	December 2015
The microbial genomics of arsenic Andres, Jérémy; Bertin, Philippe N. FEMS Microbiology Reviews, Vol. 40, Issue 2 https://doi.org/10.1093/femsre/fuv050	journal	January 2016
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Crystal structures of OrfX2 and P47 from a Botulinum neurotoxin OrfX-type gene cluster Gustafsson, Robert; Berntsson, Ronnie P-A; Martínez-Carranza, Markel FEBS Letters, Vol. 591, Issue 22 https://doi.org/10.1002/1873-3468.12889	journal	November 2017
Clostridium argentinense sp. nov.: A Genetically Homogeneous Group Composed of All Strains of Clostridium botulinum Toxin Type G and Some Nontoxigenic Strains Previously Identified as Clostridium subterminale or Clostridium hastiforme Suen, J. C.; Hatheway, C. L.; Steigerwalt, A. G. International Journal of Systematic Bacteriology, Vol. 38, Issue 4 https://doi.org/10.1099/00207713-38-4-375	journal	October 1988
Distinguishing highly-related outbreak-associated Clostridium botulinum type A(B) strains Raphael, Brian H.; Shirey, Timothy B.; Lúquez, Carolina BMC Microbiology, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2180-14-192	journal	January 2014
PHASTER: a better, faster version of the PHAST phage search tool Arndt, David; Grant, Jason R.; Marcu, Ana Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw387	journal	May 2016
Differentiating Botulinum Neurotoxin-Producing Clostridia with a Simple, Multiplex PCR Assay Williamson, Charles H. D.; Vazquez, Adam J.; Hill, Karen Applied and Environmental Microbiology, Vol. 83, Issue 18 https://doi.org/10.1128/AEM.00806-17	journal	July 2017
Notes on Bacillus Botulinus Burke, G. S. Journal of Bacteriology, Vol. 4, Issue 5 https://doi.org/10.1128/JB.4.5.555-570.1.1919	journal	January 1919
Evolution of Chromosomal Clostridium botulinum Type E Neurotoxin Gene Clusters: Evidence Provided by Their Rare Plasmid-Borne Counterparts Carter, Andrew T.; Austin, John W.; Weedmark, Kelly A. Genome Biology and Evolution, Vol. 8, Issue 3 https://doi.org/10.1093/gbe/evw017	journal	March 2016
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
Outbreak of type A foodborne botulism at a boarding school, Uganda, 2008 Viray, M. A.; Wamala, J.; Fagan, R. Epidemiology and Infection, Vol. 142, Issue 11 https://doi.org/10.1017/S0950268814000387	journal	February 2014
Snf2-family proteins: chromatin remodellers for any occasion Ryan, Daniel P.; Owen-Hughes, Tom Current Opinion in Chemical Biology, Vol. 15, Issue 5 https://doi.org/10.1016/j.cbpa.2011.07.022	journal	October 2011
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
Toxin Detection in Patients' Sera by Mass Spectrometry during Two Outbreaks of Type A Botulism in France Mazuet, Christelle; Ezan, Eric; Volland, Hervé Journal of Clinical Microbiology, Vol. 50, Issue 12 https://doi.org/10.1128/JCM.02392-12	journal	December 2012
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
Molecular Epidemiology of Infant Botulism in California and Elsewhere, 1976–2010 Dabritz, Haydee A.; Hill, Karen K.; Barash, Jason R. The Journal of Infectious Diseases, Vol. 210, Issue 11 https://doi.org/10.1093/infdis/jiu331	journal	June 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
ART: a next-generation sequencing read simulator Huang, Weichun; Li, Leping; Myers, Jason R. Bioinformatics, Vol. 28, Issue 4 https://doi.org/10.1093/bioinformatics/btr708	journal	December 2011
Genomic Characterization of Newly Completed Genomes of Botulinum Neurotoxin-Producing Species from Argentina, Australia, and Africa Smith, Theresa J.; Xie, Gary; Williamson, Charles H. D. Genome Biology and Evolution, Vol. 12, Issue 3 https://doi.org/10.1093/gbe/evaa043	journal	March 2020
Two cases of botulism Mackay-scollay, E. M. The Journal of Pathology and Bacteriology, Vol. 75, Issue 2 https://doi.org/10.1002/path.1700750235	journal	April 1958
Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution Hacker, J.; Blum-Oehler, G.; Muhldorfer, I. Molecular Microbiology, Vol. 23, Issue 6 https://doi.org/10.1046/j.1365-2958.1997.3101672.x	journal	March 1997
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
Mash: fast genome and metagenome distance estimation using MinHash Ondov, Brian D.; Treangen, Todd J.; Melsted, Páll Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-0997-x	journal	June 2016
Outbreak of botulism in Kenyan nomads Smith, D. H.; Timms, G. L.; Refai, M. Annals of Tropical Medicine & Parasitology, Vol. 73, Issue 2 https://doi.org/10.1080/00034983.1979.11687241	journal	April 1979
A framework for variation discovery and genotyping using next-generation DNA sequencing data DePristo, Mark A.; Banks, Eric; Poplin, Ryan Nature Genetics, Vol. 43, Issue 5 https://doi.org/10.1038/ng.806	journal	April 2011
Genetic Characterization and Comparison of Clostridium botulinum Isolates from Botulism Cases in Japan between 2006 and 2011 Kenri, Tsuyoshi; Sekizuka, Tsuyoshi; Yamamoto, Akihiko Applied and Environmental Microbiology, Vol. 80, Issue 22 https://doi.org/10.1128/AEM.02134-14	journal	September 2014
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
Beiträge zur Kenntnis des Toxins und Antitoxins des Bacillus botulinus Leuchs, J. Zeitschrift für Hygiene und Infektionskrankheiten, Vol. 65, Issue 1 https://doi.org/10.1007/BF02284114	journal	December 1910
Fatal type A botulism in South Africa, 2002 Frean, John; Arntzen, Lorraine; van den Heever, Johann Transactions of the Royal Society of Tropical Medicine and Hygiene, Vol. 98, Issue 5 https://doi.org/10.1016/S0035-9203(03)00069-5	journal	May 2004
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
PHYSIOLOGY OF TOXIN PRODUCTION BY CLOSTRIDIUM BOTULINUM TYPES A AND B I: Growth, Autolysis, and Toxin Production Bonventre, Peter F.; Kempe, Lloyd L. Journal of Bacteriology, Vol. 79, Issue 1 https://doi.org/10.1128/JB.79.1.18-23.1960	journal	January 1960
ModelFinder: fast model selection for accurate phylogenetic estimates Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F. Nature Methods, Vol. 14, Issue 6 https://doi.org/10.1038/nmeth.4285	journal	May 2017
Bulbar Paralysis in Cattle Due to the Action of a Toxicogenic Bacillus, with a Discussion on the Relationship of the Condition to Forage Poisoning (Botulism) Seddon, H. R. Journal of Comparative Pathology and Therapeutics, Vol. 35 https://doi.org/10.1016/S0368-1742(22)80021-7	journal	January 1922
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
Comparative Genomic Hybridization Analysis of Two Predominant Nordic Group I (Proteolytic) Clostridium botulinum Type B Clusters Lindström, Miia; Hinderink, Katja; Somervuo, Panu Applied and Environmental Microbiology, Vol. 75, Issue 9 https://doi.org/10.1128/AEM.02557-08	journal	March 2009
Distribution of Botulinum Toxin-Producing Clostridia in Soils of Argentina Lúquez, Carolina; Bianco, María I.; de Jong, Laura I. T. Applied and Environmental Microbiology, Vol. 71, Issue 7 https://doi.org/10.1128/AEM.71.7.4137-4139.2005	journal	July 2005
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
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
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data McKenna, A.; Hanna, M.; Banks, E. Genome Research, Vol. 20, Issue 9 https://doi.org/10.1101/gr.107524.110	journal	July 2010
Finished Whole-Genome Sequences of Clostridium butyricum Toxin Subtype E4 and Clostridium baratii Toxin Subtype F7 Strains Halpin, Jessica L.; Hill, Karen; Johnson, Shannon L. Genome Announcements, Vol. 5, Issue 29 https://doi.org/10.1128/genomeA.00375-17	journal	July 2017
Implications of Genome-Based Discrimination between Clostridium botulinum Group I and Clostridium sporogenes Strains for Bacterial Taxonomy Weigand, Michael R.; Pena-Gonzalez, Angela; Shirey, Timothy B. Applied and Environmental Microbiology, Vol. 81, Issue 16 https://doi.org/10.1128/AEM.01159-15	journal	June 2015
Characterization of Hemagglutinin Negative Botulinum Progenitor Toxins Kalb, Suzanne; Baudys, Jakub; Smith, Theresa Toxins, Vol. 9, Issue 6 https://doi.org/10.3390/toxins9060193	journal	June 2017
Clostridium botulinum group III: a group with dual identity shaped by plasmids, phages and mobile elements Skarin, Hanna; Håfström, Therese; Westerberg, Josefina BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-185	journal	April 2011
Immunoprecipitation of Native Botulinum Neurotoxin Complexes from Clostridium botulinum Subtype A Strains Lin, Guangyun; Tepp, William H.; Bradshaw, Marite Applied and Environmental Microbiology, Vol. 81, Issue 2 https://doi.org/10.1128/AEM.02817-14	journal	January 2015
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
PHAST: A Fast Phage Search Tool Zhou, Y.; Liang, Y.; Lynch, K. H. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr485	journal	June 2011
Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement Walker, Bruce J.; Abeel, Thomas; Shea, Terrance PLoS ONE, Vol. 9, Issue 11 https://doi.org/10.1371/journal.pone.0112963	journal	November 2014
Fast algorithms for large-scale genome alignment and comparison Delcher, A. L. Nucleic Acids Research, Vol. 30, Issue 11 https://doi.org/10.1093/nar/30.11.2478	journal	June 2002
The hypothetical protein P47 of Clostridium botulinum E1 strain Beluga has a structural topology similar to bactericidal/permeability-increasing protein Lam, Kwok-ho; Qi, Ruifeng; Liu, Shun Toxicon, Vol. 147 https://doi.org/10.1016/j.toxicon.2017.10.012	journal	June 2018
Bacteriophages of Clostridium botulinum types A, B, E, and F and nontoxigenic strains resembling type E. Eklund, M. W.; Poysky, F. T.; Boatman, E. S. Journal of Virology, Vol. 3, Issue 2 https://doi.org/10.1128/JVI.3.2.270-274.1969	journal	January 1969
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
Reoccurrence of botulinum neurotoxin subtype A3 inducing food-borne botulism, Slovakia, 2015 Mad’arová, Lucia; Dorner, Brigitte G.; Schaade, Lars Eurosurveillance, Vol. 22, Issue 32 https://doi.org/10.2807/1560-7917.ES.2017.22.32.30591	journal	August 2017

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59 BASIC BIOLOGICAL SCIENCES
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neurotoxin
plasmids
orfX
lycA
arsC
pulE

Title: 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

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