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

Weigand, Michael R.; Pena‐Gonzalez, Angela; Shirey, T. Brian; Broeker, Robin Gwen; Ishaq, Maliha K.; Konstantinidis, Konstantinos T.; Raphael, Brian

doi:10.1128/aem.01159-15

Cited by 55 publications

(78 citation statements)

References 53 publications

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“…All but one of the C. sporogenes genomes clustered in C. botulinum Group I (lineage II), together with nine C. botulinum genomes forming a more distantly related lineage ( Figure 1A , lineage II and Supplementary Table S4). It was recently reported that C. botulinum strains CDC68016, ATCC 51387, Prevot 1662, Osaka05, and Okayama2011 were defined as C. sporogenes -like strains that may have acquired a neurotoxin gene via horizontal transfer of plasmid DNA (Weigand et al, 2015). Conversely, C. sporogenes strain CDC24533 belonging to lineage I is a C. botulinum Group I strain that probably lost its neurotoxigenic plasmid (Weigand et al, 2015).…”

Section: Resultsmentioning

confidence: 99%

“…It was recently reported that C. botulinum strains CDC68016, ATCC 51387, Prevot 1662, Osaka05, and Okayama2011 were defined as C. sporogenes -like strains that may have acquired a neurotoxin gene via horizontal transfer of plasmid DNA (Weigand et al, 2015). Conversely, C. sporogenes strain CDC24533 belonging to lineage I is a C. botulinum Group I strain that probably lost its neurotoxigenic plasmid (Weigand et al, 2015). C. botulinum Group II strains were separated into two distinct lineages ( Figure 1B ; Supplementary Table S4).…”

Section: Resultsmentioning

confidence: 99%

“…C. sporogenes is a significant cause of food spoilage (McClure, 2006), and due to its close physiological similarity to C. botulinum Group I is widely used as a surrogate in demonstrating the effectiveness of food preservation processes (Brown et al, 2012; Taylor et al, 2013). Recent analysis indicates that several strains that form type B neurotoxin, and were previously classified as C. botulinum Group I, appear more like strains of C. sporogenes that have acquired a neurotoxin gene (Carter et al, 2009; Weigand et al, 2015; Williamson et al, 2016). C. botulinum Group II (non-proteolytic C. botulinum ) is an important cause of foodborne botulism in humans, and is a concern for the safe production of minimally heat-processed refrigerated foods (Peck and Stringer, 2005; Peck, 2006; Peck et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2016

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Clostridium botulinum is a highly dangerous pathogen that forms very resistant endospores that are ubiquitous in the environment, and which, under favorable conditions germinate to produce vegetative cells that multiply and form the exceptionally potent botulinum neurotoxin. To improve the control of botulinum neurotoxin-forming clostridia, it is important to understand the mechanisms involved in spore germination. Here we present models for spore germination in C. botulinum based on comparative genomics analyses, with C. botulinum Groups I and III sharing similar pathways, which differ from those proposed for C. botulinum Groups II and IV. All spores germinate in response to amino acids interacting with a germinant receptor, with four types of germinant receptor identified [encoded by various combinations of gerA, gerB, and gerC genes (gerX)]. There are three gene clusters with an ABC-like configuration; ABC [gerX1], ABABCB [gerX2] and ACxBBB [gerX4], and a single CA-B [gerX3] gene cluster. Subtypes have been identified for most germinant receptor types, and the individual GerX subunits of each cluster show similar grouping in phylogenetic trees. C. botulinum Group I contained the largest variety of gerX subtypes, with three gerX1, three gerX2, and one gerX3 subtypes, while C. botulinum Group III contained two gerX1 types and one gerX4. C. botulinum Groups II and IV contained a single germinant receptor, gerX3 and gerX1, respectively. It is likely that all four C. botulinum Groups include a SpoVA channel involved in dipicolinic acid release. The cortex-lytic enzymes present in C. botulinum Groups I and III appear to be CwlJ and SleB, while in C. botulinum Groups II and IV, SleC appears to be important.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2016

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“…However, it is now apparent that C. sporogenes is not simply a non-toxigenic version of C. botulinum Group I [5, 7•, 49•, 50]. Core genome SNP analysis reveals two clusters, that each contain strains of non-toxigenic C. sporogenes and Group I type B, distantly located from other Group I strains (lower two clusters in Figure 2, panel a).…”

Section: Genomic Diversity Of Clostridium Botulinum Group Imentioning

confidence: 99%

Impact of Clostridium botulinum genomic diversity on food safety

Peck

Vliet

2016

Current Opinion in Food Science

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“…We are currently in the process of screening clade II C. sporogenes PA 3679 isolates for C. sporogenes clade-specific genes identified by Weigand et al (24). A thorough genomic comparison between clade II isolates of C. sporogenes PA 3679 and group I C. botulinum strains to highlight the gene content differences between these organisms, especially genes that may be involved in increased spore heat resistance, is also in progress.…”

Section: Discussionmentioning

confidence: 99%

Genetic Diversity of Clostridium sporogenes PA 3679 Isolates Obtained from Different Sources as Resolved by Pulsed-Field Gel Electrophoresis and High-Throughput Sequencing

Schill

Wang

Butler

et al. 2016

Appl Environ Microbiol

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bClostridium sporogenes PA 3679 is a nonpathogenic, nontoxic model organism for proteolytic Clostridium botulinum used in the validation of conventional thermal food processes due to its ability to produce highly heat-resistant endospores. Because of its public safety importance, the uncertain taxonomic classification and genetic diversity of PA 3679 are concerns. Therefore, isolates of C. sporogenes PA 3679 were obtained from various sources and characterized using pulsed-field gel electrophoresis (PFGE) and whole-genome sequencing. The phylogenetic relatedness and genetic variability were assessed based on 16S rRNA gene sequencing and whole-genome single nucleotide polymorphism (SNP) analysis. All C. sporogenes PA 3679 isolates were categorized into two clades (clade I containing ATCC 7955 NCA3679 isolates 1961-2, 1990, and 2007 and clade II containing PA 3679 isolates NFL, UW, FDA, and Campbell and ATCC 7955 NCA3679 isolate 1961-4). The 16S maximum likelihood (ML) tree clustered both clades within proteolytic C. botulinum strains, with clade I forming a distinct cluster with other C. sporogenes non-PA 3679 strains. SNP analysis revealed that clade I isolates were more similar to the genomic reference PA 3679 (NCTC8594) genome (GenBank accession number AGAH00000000.1) than clade II isolates were. The genomic reference C. sporogenes PA 3679 (NCTC8594) genome and clade I C. sporogenes isolates were genetically distinct from those obtained from other sources (University of Wisconsin, National Food Laboratory, U.S. Food and Drug Administration, and Campbell's Soup Company). Thermal destruction studies revealed that clade I isolates were more sensitive to high temperature than clade II isolates were. Considering the widespread use of C. sporogenes PA 3679 and its genetic information in numerous studies, the accurate identification and genetic characterization of C. sporogenes PA 3679 are of critical importance. F ood-borne botulism is a neuroparalytic disease that results from the ingestion of botulinum neurotoxin (BoNT) produced by clostridia, including Clostridium botulinum and rare strains of Clostridium baratii and Clostridium butyricum. C. botulinum is a heterogeneous species comprised of four distinct groups (groups I to IV) of strains that differ based on genetic and phenotypic properties (1). Group I (proteolytic) C. botulinum strains can also be uniquely differentiated from the other groups based on their ability to form highly heat-resistant endospores. Spores of this organism are ubiquitously found in the environment and are generally presumed to be a natural contaminant of foods that come in contact with the soil (2). The geographical distribution of C. botulinum varies by serotype. For example, in the United States, spores of C. botulinum strains producing type B toxin are typically found in the soils east of the Mississippi River, and type A strains are found in the western region of the United States. Serotype E strains are commonly found in the soil sediments of the Great Lakes regions and in Alaska...

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

Cited by 55 publications

References 53 publications

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

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

Impact of Clostridium botulinum genomic diversity on food safety

Genetic Diversity of Clostridium sporogenes PA 3679 Isolates Obtained from Different Sources as Resolved by Pulsed-Field Gel Electrophoresis and High-Throughput Sequencing

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