Cereulide production by Bacillus weihenstephanensis strains during growth at different pH values and temperatures

Guerin, Alizée; Rønning, Helene Thorsen; Dargaignaratz, Claire; Clavel, Thierry; Broussolle, Véronique; Mahillon, Jacques; Granum, Per Einar; Nguyen-Thé, Christophe

doi:10.1016/j.fm.2017.02.006

Cited by 32 publications

(21 citation statements)

References 32 publications

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“…All strains of the B. cereus group (including psychrotrophic B. cereus ) appear to possess genes required to produce at least one of these diarrhoeal enterotoxins, but the extent of pathogenicity is influenced by factors such as the number and type of diarrhoeal enterotoxin genes present, their expression, and importantly the quantity of enterotoxin formed (Böhm et al, 2015; Castiaux et al, 2016; Glasset et al, 2016; Guinebretiere, Broussolle, & Nguyen-The, 2002; Guinebretière et al, 2010; Hendriksen et al, 2006; Jeβberger et al, 2015; Kovac et al, 2016; Miller, Jian, Beno, Wiedmann, & Kovac, 2018; Samapundo, Heyndrickx, et al, 2011; Stenfors, Mayr, Scherer, & Granum, 2002), and not all strains may form sufficient of the diarrhoeal enterotoxin(s) to cause foodborne illness (Miller et al, 2018; Stenfors Arnesen et al, 2008). The possession of the ces gene and the ability to form the emetic toxin (cereulide) is limited to a fraction of strains in the B. cereus group, and details are emerging of the regulation of, and environmental cues affecting emetic toxin formation, for example toxin formation is not favoured by anaerobiosis or chilled temperature (Biesta-Peters, Dissel, Reij, Zwietering, & in't Veld, 2016; Ehling-Schulz et al, 2015; Guérin, Thorsen Rønning et al, 2017). Several isoforms of cereulide have been identified, with varying potency (Marxen et al, 2015).…”

Section: Properties Of Bacillus Cereusmentioning

confidence: 99%

“…Exposure to vegetative cells is less likely to lead to diarrhoeal illness. The ability to form cereulide toxin at ≤8 °C seems to be limited to a fraction of psychrotrophic B. cereus strains, and the quantity of cereulide formed has been low (Altayar & Sutherland, 2006; Guérin, Thorsen Rønning et al, 2017; Hoton et al, 2009; Thorsen et al, 2006). The thermal processes given to minimally processed chilled foods will not inactivate cereulide, thus when food is consumed, any cereulide toxin will pass into the GI tract and potentially cause emetic illness.…”

Section: Exposure Assessmentmentioning

confidence: 99%

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Risk presented to minimally processed chilled foods by psychrotrophic Bacillus cereus

Webb

Barker

Goodburn

et al. 2019

Trends in Food Science & Technology

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BackgroundSpores of psychrotrophic Bacillus cereus may survive the mild heat treatments given to minimally processed chilled foods. Subsequent germination and cell multiplication during refrigerated storage may lead to bacterial concentrations that are hazardous to health.Scope and approachThis review is concerned with the characterisation of factors that prevent psychrotrophic B. cereus reaching hazardous concentrations in minimally processed chilled foods and associated foodborne illness. A risk assessment framework is used to quantify the risk associated with B. cereus and minimally processed chilled foods.Key findings and conclusionsBacillus cereus is responsible for two types of food poisoning, diarrhoeal (an infection) and emetic (an intoxication); however, no reported outbreaks of food poisoning have been associated with B. cereus and correctly stored commercially-produced minimally processed chilled foods. In the UK alone, more than 1010 packs of these foods have been sold in recent years without reported illness, thus the risk presented is very low. Further quantification of the risk is merited, and this requires additional data. The lack of association between diarrhoeal food poisoning and correctly stored commercially-produced minimally processed chilled foods indicates that an infectious dose has not been reached. This may reflect low pathogenicity of psychrotrophic strains. The lack of reported association of psychrotrophic B. cereus with emetic illness and correctly stored commercially-produced minimally processed chilled foods indicates that a toxic dose of the emetic toxin has not been formed. Laboratory studies show that strains form very small quantities of emetic toxin at chilled temperatures.

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Section: Properties Of Bacillus Cereusmentioning

confidence: 99%

Section: Exposure Assessmentmentioning

confidence: 99%

Risk presented to minimally processed chilled foods by psychrotrophic Bacillus cereus

Webb

Barker

Goodburn

et al. 2019

Trends in Food Science & Technology

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“…Daelman et al, show that the proper food handling is adequate to prevent illnesses caused by B. cereus [13]. Samapundo et al, showed that 88% of the isolates they studied did not grow at �8˚C [14] and Guérin A et al, showed that toxin produced by B. cereus increased 5-fold between 8˚C and 10-15˚C and by more than 100-fold between 15˚C and 25˚C while production of toxins is not favorable under anaerobic conditions [15]. Guérin A et al, 2016 shows that combinations of anaerobiosis with low pH and cold temperatures effect the growth capacities of Bacillus cereus [16].…”

Section: Introductionmentioning

confidence: 99%

Quantitative bioluminescence assay for measuring Bacillus cereus nonhemolytic enterotoxin complex

2020

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Bacillus cereus is a foodborne pathogen causing emesis and diarrhea in those affected. It is assumed that the non-hemolytic enterotoxin (Nhe) plays a key role in B. cereus induced diarrhea. The ability to trace Nhe activity is important for food safety. While assays such as PCR and ELISA exist to detect Nhe, those methods cannot differentiate between active and inactive forms of Nhe. The existing rabbit ileal loop bioassay used to detect Nhe activity is ethically disfavored because it uses live experimental animals. Here we present a custom built low-cost CCD based luminometer and applied it in conjunction with a cell-based assay using Vero cells transduced to express the luciferase enzyme. The activity of Nhe was measured as its ability to inhibit synthesis of luciferase as quantified by reduction of light emission by the luciferase reaction. Emitted light intensity was observed to be inversely proportional to Nhe concentration over a range of 7 ng/ml to 125 ng/ml, with a limit of detection of 7 ng/ml Nhe.

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“…Production of cereulide, the toxin responsible for emetic B. cereus foodborne illness, can be attributed to cereulide synthetase, a nonribosomal peptide synthetase encoded by the cereulide synthetase biosynthetic gene cluster (ces) (9,10). ces has been detected in two major B. cereus sensu lato phylogenetic groups (assigned using the sequence of pantoate-beta-alanine ligase [panC] and a seven-group typing scheme): group III and group VI (10)(11)(12)(13)(14)(15)(16). While cereulide-producing group VI strains, also known as "emetic B. weihenstephanensis," have been isolated on rare occasions (14,15,(17)(18)(19), the bulk of cereulide-producing strains belong to group III (8,10,13,16).…”

mentioning

confidence: 99%

“…ces has been detected in two major B. cereus sensu lato phylogenetic groups (assigned using the sequence of pantoate-beta-alanine ligase [panC] and a seven-group typing scheme): group III and group VI (10)(11)(12)(13)(14)(15)(16). While cereulide-producing group VI strains, also known as "emetic B. weihenstephanensis," have been isolated on rare occasions (14,15,(17)(18)(19), the bulk of cereulide-producing strains belong to group III (8,10,13,16). Often referred to as "emetic B. cereus," cereulide-producing group III strains often harbor ces on plasmids (9,10,19) and have been linked to outbreaks around the world (5,7,8,20).…”

mentioning

confidence: 99%

Cereulide Synthetase Acquisition and Loss Events within the Evolutionary History of Group III Bacillus cereus Sensu Lato Facilitate the Transition between Emetic and Diarrheal Foodborne Pathogens

Carroll

2020

mBio

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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.

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Cereulide production by Bacillus weihenstephanensis strains during growth at different pH values and temperatures

Cited by 32 publications

References 32 publications

Risk presented to minimally processed chilled foods by psychrotrophic Bacillus cereus

Risk presented to minimally processed chilled foods by psychrotrophic Bacillus cereus

Quantitative bioluminescence assay for measuring Bacillus cereus nonhemolytic enterotoxin complex

Cereulide Synthetase Acquisition and Loss Events within the Evolutionary History of Group III Bacillus cereus Sensu Lato Facilitate the Transition between Emetic and Diarrheal Foodborne Pathogens

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