Cytotoxicity and Genome Characteristics of an Emetic Toxin-Producing Bacillus cereus Group sp. Isolated from Raw Milk

The Bacillus cereus group frequently contaminates milk and dairy products. Some members of this group can produce the heat-stable pre-formed toxin cereulide, which causes emetic foodborne intoxication. This study characterised emetic B. cereus group isolates from raw cow’s milk in the biochemical, g...

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Published inFoods Vol. 14; no. 3; p. 485
Main Authors Pheepakpraw, Jintana, Sinchao, Chanita, Sutheeworapong, Sawannee, Sattayawat, Pachara, Panya, Aussara, Tragoolpua, Yingmanee, Chitov, Thararat
Format Journal Article
LanguageEnglish
Published Switzerland MDPI AG 03.02.2025
MDPI
Subjects
Bacillus cereus
Bacillus cereus group
Carbohydrates
Cell culture
Cereulide
Cow's milk
Cytotoxicity
dairy
Dairy industry
Dairy products
DNA polymerase
emetic toxin
Enzymes
Ethylenediaminetetraacetic acid
Food contamination & poisoning
food safety
Genes
Genetic analysis
genome sequencing
Genomes
Genomic analysis
Genomics
Heat treatment
Intoxication
Ligases
Milk
Peptides
Phenotypes
Proteins
Single-nucleotide polymorphism
Thermal stability
Toxicity
Toxins
Virulence (Microbiology)
Virulence factors
Thailand
United States
Massachusetts
Malaysia
France
Detroit Michigan
United States > US
food safety
genome sequencing
Bacillus cereus group
emetic toxin
dairy
cereulide
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Abstract The Bacillus cereus group frequently contaminates milk and dairy products. Some members of this group can produce the heat-stable pre-formed toxin cereulide, which causes emetic foodborne intoxication. This study characterised emetic B. cereus group isolates from raw cow’s milk in the biochemical, genetic, and toxigenic aspects. Of the 158 B. cereus group isolates derived from 99 raw milk samples, 7 (4.43%) harboured cereulide synthetase A (cesA), which encodes a cereulide synthetase associated with the emetic phenotype. Heat-treated culture filtrates from the cesA-positive isolates demonstrated cytotoxicity to HepG2 and Caco-2 cells, resulting in cell viabilities of 32.22–36.57% and 44.41–47.08%, respectively. The cytotoxicity levels were comparable to those of the reference emetic strain, F4810/72 (alternately termed AH187). Genome analysis of a representative isolate, CSB98, revealed the complete ces gene cluster with additional virulence factors such as non-haemolytic enterotoxin, haemolysins and phospholipases, suggesting that the isolate could be both emetic and diarrhoeagenic. CSB98 exhibited a closer relationship to the type strain of B. paranthracis than to that of B. cereus sensu stricto (ATCC 14579). The genomes of CSB98 and AH187 were indistinguishable through OrthoANI analysis, but 13 variants were identified via SNP calling. These results affirm genetic conservation among the emetic traits.
AbstractList The Bacillus cereus group frequently contaminates milk and dairy products. Some members of this group can produce the heat-stable pre-formed toxin cereulide, which causes emetic foodborne intoxication. This study characterised emetic B. cereus group isolates from raw cow’s milk in the biochemical, genetic, and toxigenic aspects. Of the 158 B. cereus group isolates derived from 99 raw milk samples, 7 (4.43%) harboured cereulide synthetase A (cesA), which encodes a cereulide synthetase associated with the emetic phenotype. Heat-treated culture filtrates from the cesA-positive isolates demonstrated cytotoxicity to HepG2 and Caco-2 cells, resulting in cell viabilities of 32.22–36.57% and 44.41–47.08%, respectively. The cytotoxicity levels were comparable to those of the reference emetic strain, F4810/72 (alternately termed AH187). Genome analysis of a representative isolate, CSB98, revealed the complete ces gene cluster with additional virulence factors such as non-haemolytic enterotoxin, haemolysins and phospholipases, suggesting that the isolate could be both emetic and diarrhoeagenic. CSB98 exhibited a closer relationship to the type strain of B. paranthracis than to that of B. cereus sensu stricto (ATCC 14579). The genomes of CSB98 and AH187 were indistinguishable through OrthoANI analysis, but 13 variants were identified via SNP calling. These results affirm genetic conservation among the emetic traits.
The Bacillus cereus group frequently contaminates milk and dairy products. Some members of this group can produce the heat-stable pre-formed toxin cereulide, which causes emetic foodborne intoxication. This study characterised emetic B. cereus group isolates from raw cow's milk in the biochemical, genetic, and toxigenic aspects. Of the 158 B. cereus group isolates derived from 99 raw milk samples, 7 (4.43%) harboured cereulide synthetase A (cesA), which encodes a cereulide synthetase associated with the emetic phenotype. Heat-treated culture filtrates from the cesA-positive isolates demonstrated cytotoxicity to HepG2 and Caco-2 cells, resulting in cell viabilities of 32.22-36.57% and 44.41-47.08%, respectively. The cytotoxicity levels were comparable to those of the reference emetic strain, F4810/72 (alternately termed AH187). Genome analysis of a representative isolate, CSB98, revealed the complete ces gene cluster with additional virulence factors such as non-haemolytic enterotoxin, haemolysins and phospholipases, suggesting that the isolate could be both emetic and diarrhoeagenic. CSB98 exhibited a closer relationship to the type strain of B. paranthracis than to that of B. cereus sensu stricto (ATCC 14579). The genomes of CSB98 and AH187 were indistinguishable through OrthoANI analysis, but 13 variants were identified via SNP calling. These results affirm genetic conservation among the emetic traits.The Bacillus cereus group frequently contaminates milk and dairy products. Some members of this group can produce the heat-stable pre-formed toxin cereulide, which causes emetic foodborne intoxication. This study characterised emetic B. cereus group isolates from raw cow's milk in the biochemical, genetic, and toxigenic aspects. Of the 158 B. cereus group isolates derived from 99 raw milk samples, 7 (4.43%) harboured cereulide synthetase A (cesA), which encodes a cereulide synthetase associated with the emetic phenotype. Heat-treated culture filtrates from the cesA-positive isolates demonstrated cytotoxicity to HepG2 and Caco-2 cells, resulting in cell viabilities of 32.22-36.57% and 44.41-47.08%, respectively. The cytotoxicity levels were comparable to those of the reference emetic strain, F4810/72 (alternately termed AH187). Genome analysis of a representative isolate, CSB98, revealed the complete ces gene cluster with additional virulence factors such as non-haemolytic enterotoxin, haemolysins and phospholipases, suggesting that the isolate could be both emetic and diarrhoeagenic. CSB98 exhibited a closer relationship to the type strain of B. paranthracis than to that of B. cereus sensu stricto (ATCC 14579). The genomes of CSB98 and AH187 were indistinguishable through OrthoANI analysis, but 13 variants were identified via SNP calling. These results affirm genetic conservation among the emetic traits.
The Bacillus cereus group frequently contaminates milk and dairy products. Some members of this group can produce the heat-stable pre-formed toxin cereulide, which causes emetic foodborne intoxication. This study characterised emetic B. cereus group isolates from raw cow’s milk in the biochemical, genetic, and toxigenic aspects. Of the 158 B. cereus group isolates derived from 99 raw milk samples, 7 (4.43%) harboured cereulide synthetase A ( cesA ), which encodes a cereulide synthetase associated with the emetic phenotype. Heat-treated culture filtrates from the cesA -positive isolates demonstrated cytotoxicity to HepG2 and Caco-2 cells, resulting in cell viabilities of 32.22–36.57% and 44.41–47.08%, respectively. The cytotoxicity levels were comparable to those of the reference emetic strain, F4810/72 (alternately termed AH187). Genome analysis of a representative isolate, CSB98, revealed the complete ces gene cluster with additional virulence factors such as non-haemolytic enterotoxin, haemolysins and phospholipases, suggesting that the isolate could be both emetic and diarrhoeagenic. CSB98 exhibited a closer relationship to the type strain of B. paranthracis than to that of B. cereus sensu stricto (ATCC 14579). The genomes of CSB98 and AH187 were indistinguishable through OrthoANI analysis, but 13 variants were identified via SNP calling. These results affirm genetic conservation among the emetic traits.
The group frequently contaminates milk and dairy products. Some members of this group can produce the heat-stable pre-formed toxin cereulide, which causes emetic foodborne intoxication. This study characterised emetic group isolates from raw cow's milk in the biochemical, genetic, and toxigenic aspects. Of the 158 group isolates derived from 99 raw milk samples, 7 (4.43%) harboured ( ), which encodes a cereulide synthetase associated with the emetic phenotype. Heat-treated culture filtrates from the -positive isolates demonstrated cytotoxicity to HepG2 and Caco-2 cells, resulting in cell viabilities of 32.22-36.57% and 44.41-47.08%, respectively. The cytotoxicity levels were comparable to those of the reference emetic strain, F4810/72 (alternately termed AH187). Genome analysis of a representative isolate, CSB98, revealed the complete gene cluster with additional virulence factors such as non-haemolytic enterotoxin, haemolysins and phospholipases, suggesting that the isolate could be both emetic and diarrhoeagenic. CSB98 exhibited a closer relationship to the type strain of than to that of (ATCC 14579). The genomes of CSB98 and AH187 were indistinguishable through OrthoANI analysis, but 13 variants were identified via SNP calling. These results affirm genetic conservation among the emetic traits.
Audience Academic
Author Sutheeworapong, Sawannee
Pheepakpraw, Jintana
Panya, Aussara
Sinchao, Chanita
Tragoolpua, Yingmanee
Sattayawat, Pachara
Chitov, Thararat
AuthorAffiliation 2 Doctor of Philosophy Program in Applied Microbiology (International Program), Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
3 Systems Biology and Bioinformatics Laboratory, Pilot Plant Development and Training Institute, King Mongkut’s University of Technology Thonburi, Bangkok 10150, Thailand; sawannee.sut@kmutt.ac.th
1 Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand; jintana_ph@cmu.ac.th (J.P.); chanita_sin@cmu.ac.th (C.S.); pachara.sattayawat@cmu.ac.th (P.S.); aussara.pan@cmu.ac.th (A.P.); yingmanee.t@cmu.ac.th (Y.T.)
4 Environmental Science Research Center (ESRC), Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
AuthorAffiliation_xml – name: 3 Systems Biology and Bioinformatics Laboratory, Pilot Plant Development and Training Institute, King Mongkut’s University of Technology Thonburi, Bangkok 10150, Thailand; sawannee.sut@kmutt.ac.th
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– name: 1 Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand; jintana_ph@cmu.ac.th (J.P.); chanita_sin@cmu.ac.th (C.S.); pachara.sattayawat@cmu.ac.th (P.S.); aussara.pan@cmu.ac.th (A.P.); yingmanee.t@cmu.ac.th (Y.T.)
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Issue 3
Keywords food safety
genome sequencing
Bacillus cereus group
emetic toxin
dairy
cereulide
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Snippet The Bacillus cereus group frequently contaminates milk and dairy products. Some members of this group can produce the heat-stable pre-formed toxin cereulide,...
The group frequently contaminates milk and dairy products. Some members of this group can produce the heat-stable pre-formed toxin cereulide, which causes...
The Bacillus cereus group frequently contaminates milk and dairy products. Some members of this group can produce the heat-stable pre-formed toxin cereulide,...
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StartPage 485
SubjectTerms Bacillus cereus
Bacillus cereus group
Carbohydrates
Cell culture
Cereulide
Cow's milk
Cytotoxicity
dairy
Dairy industry
Dairy products
DNA polymerase
emetic toxin
Enzymes
Ethylenediaminetetraacetic acid
Food contamination & poisoning
food safety
Genes
Genetic analysis
genome sequencing
Genomes
Genomic analysis
Genomics
Heat treatment
Intoxication
Ligases
Milk
Peptides
Phenotypes
Proteins
Single-nucleotide polymorphism
Thermal stability
Toxicity
Toxins
Virulence (Microbiology)
Virulence factors
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Title Cytotoxicity and Genome Characteristics of an Emetic Toxin-Producing Bacillus cereus Group sp. Isolated from Raw Milk
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Volume 14
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