Cereulide Synthetase Acquisition and Loss Events within the Evolutionary History of Group III <italic toggle="yes">Bacillus cereus Sensu Lato</italic> Facilitate the Transition between Emetic and Diarrheal Foodborne Pathogens

ABSTRACT Cereulide-producing members of Bacillus cereus sensu lato group III (also known as emetic B. cereus) possess cereulide synthetase, a plasmid-encoded, nonribosomal peptide synthetase encoded by the ces gene cluster. Despite the documented risks that cereulide-producing strains pose to public...

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Autores principales:	Laura M. Carroll, Martin Wiedmann
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Bacillus Emeticus Bacillus cereus emetic Bacillus cereus cereulide foodborne illness genomic epidemiology Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ff0d2cda443e486abe935178e99c4c18
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spelling	oai:doaj.org-article:ff0d2cda443e486abe935178e99c4c182021-11-15T15:56:44ZCereulide Synthetase Acquisition and Loss Events within the Evolutionary History of Group III <italic toggle="yes">Bacillus cereus Sensu Lato</italic> Facilitate the Transition between Emetic and Diarrheal Foodborne Pathogens10.1128/mBio.01263-202150-7511https://doaj.org/article/ff0d2cda443e486abe935178e99c4c182020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01263-20https://doaj.org/toc/2150-7511ABSTRACT Cereulide-producing members of Bacillus cereus sensu lato group III (also known as emetic B. cereus) possess cereulide synthetase, a plasmid-encoded, nonribosomal peptide synthetase encoded by the ces gene cluster. Despite the documented risks that cereulide-producing strains pose to public health, the level of genomic diversity encompassed by emetic B. cereus has never been evaluated at a whole-genome scale. Here, we employ a phylogenomic approach to characterize group III B. cereus sensu lato genomes which possess ces (ces positive) alongside their closely related, ces-negative counterparts (i) to assess the genomic diversity encompassed by emetic B. cereus and (ii) to identify potential ces loss and/or gain events within the evolutionary history of the high-risk and medically relevant sequence type (ST) 26 lineage often associated with emetic foodborne illness. Using all publicly available ces-positive group III B. cereus sensu lato genomes and the ces-negative genomes interspersed among them (n = 159), we show that emetic B. cereus is not clonal; rather, multiple lineages within group III harbor cereulide-producing strains, all of which share an ancestor incapable of producing cereulide (posterior probability = 0.86 to 0.89). Members of ST 26 share an ancestor that existed circa 1748 (95% highest posterior density [HPD] interval = 1246.89 to 1915.64) and first acquired the ability to produce cereulide before 1876 (95% HPD = 1641.43 to 1946.70). Within ST 26 alone, two subsequent ces gain events were observed, as well as three ces loss events, including among isolates responsible for B. cereus sensu lato toxicoinfection (i.e., “diarrheal” illness). IMPORTANCE B. cereus is responsible for thousands of cases of foodborne disease each year worldwide, causing two distinct forms of illness: (i) intoxication via cereulide (i.e., emetic syndrome) or (ii) toxicoinfection via multiple enterotoxins (i.e., diarrheal syndrome). Here, we show that emetic B. cereus is not a clonal, homogenous unit that resulted from a single cereulide synthetase gain event followed by subsequent proliferation; rather, cereulide synthetase acquisition and loss is a dynamic, ongoing process that occurs across lineages, allowing some group III B. cereus sensu lato populations to oscillate between diarrheal and emetic foodborne pathogens over the course of their evolutionary histories. We also highlight the care that must be taken when selecting a reference genome for whole-genome sequencing-based investigation of emetic B. cereus sensu lato outbreaks, since some reference genome selections can lead to a confounding loss of resolution and potentially hinder epidemiological investigations.Laura M. CarrollMartin WiedmannAmerican Society for MicrobiologyarticleBacillus EmeticusBacillus cereusemetic Bacillus cereuscereulidefoodborne illnessgenomic epidemiologyMicrobiologyQR1-502ENmBio, Vol 11, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacillus Emeticus Bacillus cereus emetic Bacillus cereus cereulide foodborne illness genomic epidemiology Microbiology QR1-502
spellingShingle	Bacillus Emeticus Bacillus cereus emetic Bacillus cereus cereulide foodborne illness genomic epidemiology Microbiology QR1-502 Laura M. Carroll Martin Wiedmann Cereulide Synthetase Acquisition and Loss Events within the Evolutionary History of Group III <italic toggle="yes">Bacillus cereus Sensu Lato</italic> Facilitate the Transition between Emetic and Diarrheal Foodborne Pathogens
description	ABSTRACT Cereulide-producing members of Bacillus cereus sensu lato group III (also known as emetic B. cereus) possess cereulide synthetase, a plasmid-encoded, nonribosomal peptide synthetase encoded by the ces gene cluster. Despite the documented risks that cereulide-producing strains pose to public health, the level of genomic diversity encompassed by emetic B. cereus has never been evaluated at a whole-genome scale. Here, we employ a phylogenomic approach to characterize group III B. cereus sensu lato genomes which possess ces (ces positive) alongside their closely related, ces-negative counterparts (i) to assess the genomic diversity encompassed by emetic B. cereus and (ii) to identify potential ces loss and/or gain events within the evolutionary history of the high-risk and medically relevant sequence type (ST) 26 lineage often associated with emetic foodborne illness. Using all publicly available ces-positive group III B. cereus sensu lato genomes and the ces-negative genomes interspersed among them (n = 159), we show that emetic B. cereus is not clonal; rather, multiple lineages within group III harbor cereulide-producing strains, all of which share an ancestor incapable of producing cereulide (posterior probability = 0.86 to 0.89). Members of ST 26 share an ancestor that existed circa 1748 (95% highest posterior density [HPD] interval = 1246.89 to 1915.64) and first acquired the ability to produce cereulide before 1876 (95% HPD = 1641.43 to 1946.70). Within ST 26 alone, two subsequent ces gain events were observed, as well as three ces loss events, including among isolates responsible for B. cereus sensu lato toxicoinfection (i.e., “diarrheal” illness). IMPORTANCE B. cereus is responsible for thousands of cases of foodborne disease each year worldwide, causing two distinct forms of illness: (i) intoxication via cereulide (i.e., emetic syndrome) or (ii) toxicoinfection via multiple enterotoxins (i.e., diarrheal syndrome). Here, we show that emetic B. cereus is not a clonal, homogenous unit that resulted from a single cereulide synthetase gain event followed by subsequent proliferation; rather, cereulide synthetase acquisition and loss is a dynamic, ongoing process that occurs across lineages, allowing some group III B. cereus sensu lato populations to oscillate between diarrheal and emetic foodborne pathogens over the course of their evolutionary histories. We also highlight the care that must be taken when selecting a reference genome for whole-genome sequencing-based investigation of emetic B. cereus sensu lato outbreaks, since some reference genome selections can lead to a confounding loss of resolution and potentially hinder epidemiological investigations.
format	article
author	Laura M. Carroll Martin Wiedmann
author_facet	Laura M. Carroll Martin Wiedmann
author_sort	Laura M. Carroll
title	Cereulide Synthetase Acquisition and Loss Events within the Evolutionary History of Group III <italic toggle="yes">Bacillus cereus Sensu Lato</italic> Facilitate the Transition between Emetic and Diarrheal Foodborne Pathogens
title_short	Cereulide Synthetase Acquisition and Loss Events within the Evolutionary History of Group III <italic toggle="yes">Bacillus cereus Sensu Lato</italic> Facilitate the Transition between Emetic and Diarrheal Foodborne Pathogens
title_full	Cereulide Synthetase Acquisition and Loss Events within the Evolutionary History of Group III <italic toggle="yes">Bacillus cereus Sensu Lato</italic> Facilitate the Transition between Emetic and Diarrheal Foodborne Pathogens
title_fullStr	Cereulide Synthetase Acquisition and Loss Events within the Evolutionary History of Group III <italic toggle="yes">Bacillus cereus Sensu Lato</italic> Facilitate the Transition between Emetic and Diarrheal Foodborne Pathogens
title_full_unstemmed	Cereulide Synthetase Acquisition and Loss Events within the Evolutionary History of Group III <italic toggle="yes">Bacillus cereus Sensu Lato</italic> Facilitate the Transition between Emetic and Diarrheal Foodborne Pathogens
title_sort	cereulide synthetase acquisition and loss events within the evolutionary history of group iii <italic toggle="yes">bacillus cereus sensu lato</italic> facilitate the transition between emetic and diarrheal foodborne pathogens
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/ff0d2cda443e486abe935178e99c4c18
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Cereulide Synthetase Acquisition and Loss Events within the Evolutionary History of Group III <italic toggle="yes">Bacillus cereus Sensu Lato</italic> Facilitate the Transition between Emetic and Diarrheal Foodborne Pathogens

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