Abstract
Clostridium botulinum produces the botulinum neurotoxin that causes botulism, a rare but potentially lethal paralysis. Endospores play an important role in the survival, transmission, and pathogenesis of C. botulinum. C. botulinum strains are very diverse, both genetically and ecologically. Group I strains are terrestrial, mesophilic, and produce highly heat-resistant spores, while Group II strains can be terrestrial (type B) or aquatic (type E) and are generally psychrotrophic and produce spores of moderate heat resistance. Group III strains are either terrestrial or aquatic, mesophilic or slightly thermophilic, and the heat resistance properties of their spores are poorly characterized. Here, we analyzed the sporulation dynamics in population, spore morphology, and other spore properties of 10 C. botulinum strains belonging to Groups I–III. We propose two distinct sporulation strategies used by C. botulinum Groups I–III strains, report their spore properties, and suggest a putative role for the exosporium in conferring high heat resistance. Strains within each physiological group produced spores with similar characteristics, likely reflecting adaptation to respective environmental habitats. Our work provides new information on the spores and on the population and single-cell level strategies in the sporulation of C. botulinum.
Highlights
The endospore-forming, bacterial species Clostridium botulinum is divided into phylogenetically and ecologically distinct groups of clostridia that produce the highly potent botulinum neurotoxin (BoNT) [1]
We propose two distinct sporulation strategies used by C. botulinum Groups I–III strains, report their spore properties, and suggest a putative role for the exosporium in conferring high heat resistance
While BoNT is the causative agent of botulism, C. botulinum spores play a key role in the survival and dispersion of C. botulinum in the environment, in contamination of food and feed raw materials [3,4,5,6], and in pathogenesis [1,7]
Summary
The endospore-forming, bacterial species Clostridium botulinum is divided into phylogenetically and ecologically distinct groups of clostridia that produce the highly potent botulinum neurotoxin (BoNT) [1]. The forespore is engulfed and surrounded by protective layers by the enveloping mother cell These layers determine the spore properties, resistance, and how it interacts with its environment [16]. Hydrophobic bonds allow the spore to interact with other particles or surfaces and promote active adherence [33,34] Autoaggregation is another trait associated with pathogenic adhesion and host colonization [35,36]. We analyzed the sporulation diversity of 10 C. botulinum Group I, II, or III strains by looking at (i) dynamics in the population structure in sporulating cultures and (ii) the ultrastructure and (iii) functional properties of individual spores. We report two distinct population dynamic patterns in sporulation, which could relate to the proteolytic properties of the strains of different Groups. Strains with the lowest heat resistance within their respective group either lacked an exosporium or had a thinner exosporium compared to their phylogenetically related counterparts, suggesting a possible role of the exosporium in heat resistance
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