Diversity of the Genomes and Neurotoxins of Strains of Clostridium botulinum Group I and Clostridium sporogenes Associated with Foodborne, Infant and Wound Botulism.

Jason Brunt,Andrew T Carter,Arnoud H M Van Vliet,Corinne Amar,Sandra C Stringer,Kathie A Grant,Gauri Godbole,Michael W Peck

doi:10.3390/toxins12090586

Abstract

Clostridium botulinum Group I and Clostridium sporogenes are closely related bacteria responsible for foodborne, infant and wound botulism. A comparative genomic study with 556 highly diverse strains of C. botulinum Group I and C. sporogenes (including 417 newly sequenced strains) has been carried out to characterise the genetic diversity and spread of these bacteria and their neurotoxin genes. Core genome single-nucleotide polymorphism (SNP) analysis revealed two major lineages; C. botulinum Group I (most strains possessed botulinum neurotoxin gene(s) of types A, B and/or F) and C. sporogenes (some strains possessed a type B botulinum neurotoxin gene). Both lineages contained strains responsible for foodborne, infant and wound botulism. A new C. sporogenes cluster was identified that included five strains with a gene encoding botulinum neurotoxin sub-type B1. There was significant evidence of horizontal transfer of botulinum neurotoxin genes between distantly related bacteria. Population structure/diversity have been characterised, and novel associations discovered between whole genome lineage, botulinum neurotoxin sub-type variant, epidemiological links to foodborne, infant and wound botulism, and geographic origin. The impact of genomic and physiological variability on the botulism risk has been assessed. The genome sequences are a valuable resource for future research (e.g., pathogen biology, evolution of C. botulinum and its neurotoxin genes, improved pathogen detection and discrimination), and support enhanced risk assessments and the prevention of botulism.

Highlights

Clostridium botulinum Group I and Clostridium sporogenes are closely related mesophilic bacteria that share genotypic and physiological characteristics, including a highly proteolytic nature and the ability to form spores of high thermal resistance
The genomic diversity, phylogenetic relationship and botulinum neurotoxin genes/clusters have been characterised for 556 strains of C. botulinum Group I and C. sporogenes (Table S1)
Genetic analysis carried out previously and in the present study showed that the botulinum neurotoxin genes encoded by C. sporogenes are primarily carried on a plasmid [8,22,24,25,44,91,92]

Summary

Introduction

Clostridium botulinum Group I ( known as proteolytic C. botulinum) and Clostridium sporogenes are closely related mesophilic bacteria that share genotypic and physiological characteristics, including a highly proteolytic nature and the ability to form spores of high thermal resistance. C. sporogenes has often been perceived as a non-toxic close relative of C. botulinum Group I [6,7,8,9,10,11,12,13]. It is an important cause of food spoilage [14,15,16], and used as a surrogate for C. botulinum Group I in food sterilisation tests [7,14,15,17,18,19,20]. Genetic analysis has revealed that both C. botulinum Group I and

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