Common occurrence of enterotoxin genes and enterotoxicity in<i>Bacillus thuringiensis</i>

Rivera, Adelaida María Gaviria; Granum, Per Einar; Priest, Fergus G.

doi:10.1111/j.1574-6968.2000.tb09278.x

Cited by 101 publications

(19 citation statements)

References 32 publications

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“…The nheABC operon occurrence in NCBI database is 46.6% (81/174). And the mean value frequency of nheA, nheB, nheC found in the literature is 82, 81 and 78%, respectively (Swiecicka et al 2006; Gaviria et al 2000; Hansen and Hendriksen 2001; Banerjee et al 2011; Moravek et al 2004; De Jonghe et al 2010; Krause et al 2010; Zhou et al 2010; Samapundo et al 2011; Chon et al 2015). These frequencies are slightly higher than the ratio we measured from database.…”

Section: Resultsmentioning

confidence: 96%

Genetic and genomic diversity of NheABC locus from Bacillus strains

Cai

Huang

et al. 2017

Arch Microbiol

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Non-hemolytic enterotoxin (NHE), a tri-partite, proteinaceous toxin encoded by contiguous nheA, nheB and nheC genes of Bacillus cereus sensu lato (B. cereus s.l.), is considered to be associated with the foodborne diarrheic syndrome. However, B. cereus s.l. includes a number of closely related strains, and the occurrence of NHE among them, and other members of Bacillus is unclear. Consequently, we aimed to determine the distribution and evolution of NHE within Bacillus by confirming the presence of the nheA, B and C sequences and variation within them using published data, and to analyze the genomic and genetic diversity. The phylogenetic tree of NHE proteins (NheA, NheB and NheC) from 81 different B. cereus s.l. strains was constructed. And on the genetic determinants of the NHE toxin did not bring any obvious link between the nheABC genes sequence of a strain and its virulence in the diarrhoeal pathogenesis. Analysis of the genomic diversity of the nheA, B and C loci revealed that their upstream regions were more conserved than the downstream sequences. Multilocus sequence typing schemes (MLST) based on seven concatenated housekeeping genes and nheA, B and C genes of the 75 strains were developed. The neighbor joining phylogenetic tree based on seven housekeeping genes together with nheA, B and C genes was similiar to published Bacillus phylogenetic trees. And on the genetic determinants of the NHE toxin did not bring any obvious link between the nheABC genes sequence of a strain and its virulence in the diarrhoeal pathogenesis.The results indicate that nheA, B and C genes do not affect the diversity of housekeeping genes, and this specific NHE protein does not participate in the diarrheic syndrome.Electronic supplementary materialThe online version of this article (doi:10.1007/s00203-017-1350-9) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 96%

Genetic and genomic diversity of NheABC locus from Bacillus strains

Cai

Huang

et al. 2017

Arch Microbiol

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“…While B. anthracis is considered non-enteropathogenic due to the deactivated PlcR-regulon [ 57 ], B. cereus and B. thuringiensis are known to be enterotoxic [ 48 , 65 ]. B. weihenstephanensis strains also carry enterotoxin genes.…”

Section: Resultsmentioning

confidence: 99%

Massive horizontal gene transfer, strictly vertical inheritance and ancient duplications differentially shape the evolution of Bacillus cereus enterotoxin operons hbl, cytK and nhe

et al. 2015

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BackgroundBacillus cereus sensu lato comprises eight closely related species including the human pathogens Bacillus anthracis and Bacillus cereus. Within B. cereus sensu lato, chromosomally and plasmid-encoded toxins exist. While plasmid-mediated horizontal gene transfer of the emetic toxin, anthrax and insecticidal toxins is known, evolution of enterotoxin genes within the group has not been studied.ResultsWe report draft genome assemblies of 25 strains, a phylogenetic network of 142 strains based on ANI derived from genome sequences and a phylogeny based on whole-genome SNP analysis. The data clearly support subdivision of B. cereus sensu lato into seven phylogenetic groups. While group I, V and VII represent B. pseudomycoides, B. toyonensis and B. cytotoxicus, which are distinguishable at species level (ANI border ≥ 96 %), strains ascribed to the other five species do not match phylogenic groups. The chromosomal enterotoxin operons nheABC and hblCDAB are abundant within B. cereus both isolated from infections and from the environment. While the duplicated hbl variant hbla is present in 22 % of all strains investigated, duplication of nheABC is extremely rare (0.02 %) and appears to be phylogenetically unstable. Distribution of toxin genes was matched to a master tree based on seven concatenated housekeeping genes, which depicts species relationships in B. cereus sensu lato as accurately as whole-genome comparisons. Comparison to the phylogeny of enterotoxin genes uncovered ample evidence for horizontal transfer of hbl, cytK and plcR, as well as frequent deletion of both toxins and duplication of hbl. No evidence for nhe deletion was found and stable horizontal transfer of nhe is rare. Therefore, evolution of B. cereus enterotoxin operons is shaped unexpectedly different for yet unknown reasons.ConclusionsFrequent exchange of the pathogenicity factors hbl, cytK and plcR in B. cereus sensu lato appears to be an important mechanism of B. cereus virulence evolution, including so-called probiotic or non-pathogenic species, which might have consequences for risk assessment procedures. In contrast, exclusively vertical inheritance of nhe was observed, and since nhe-negative strains appear to be extremely rare, we suggest that fitness loss may be associated with deletion or horizontal transfer of the nhe operon.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0529-4) contains supplementary material, which is available to authorized users.

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“…Since B. thuringiensis has been reported to produce enterotoxins (Griffiths, 1990 ; Damgaard et al, 1996 ; Gaviria Rivera et al, 2000 ) and is routinely not differentiated from B. cereus s.s . by diagnostic laboratories, some outbreaks of food poisoning attributed to B. cereus may in fact have been caused by B. thuringiensis .…”

Section: Introductionmentioning

confidence: 99%

“…Data on B. thuringiensis enterotoxin production generated using bioassays are scarce. Damgaard et al ( 1996 ) and Gaviria Rivera et al ( 2000 ) were able to show that culture supernatants of B. thuringiensis isolates inhibited [ 14 C]-leucine uptake in a Vero cell assay. However, the authors only included three biopesticide strains HD-1 (serotype kurstaki ), HD-567 (serotype israelensis ), and NB-125 (serotype tenebrionis ).…”

Section: Introductionmentioning

confidence: 99%

Enterotoxin Production of Bacillus thuringiensis Isolates From Biopesticides, Foods, and Outbreaks

et al. 2018

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While the relevance of Bacillus (B.) cereus as a major cause of gastroenteritis is undisputed, the role of the closely related B. thuringiensis in foodborne disease is unclear. B. thuringiensis strains frequently harbor enterotoxin genes. However, the organism has only very rarely been associated with foodborne outbreaks, possibly due to the fact that during outbreak investigations, B. cereus is routinely not differentiated from B. thuringiensis. A recent EFSA scientific opinion stresses the urgent need for further data allowing for improved risk assessment, in particular as B. thuringiensis is a commonly used biopesticide. Therefore, the aim of this study was to gain further insights into the hazardous potential of B. thuringiensis. To this end, 39 B. thuringiensis isolates obtained from commercially used biopesticides, various food sources, as well as from foodborne outbreaks were characterized by panC typing, panC-based SplitsTree analysis, toxin gene profiling, FTIR spectroscopic analysis, a cytotoxicity assay screening for enterotoxic activity, and a sphingomyelinase assay. The majority of the tested B. thuringiensis isolates exhibited low (23%, n = 9) or mid level enterotoxicity (74%, n = 29), and produced either no (59%, n = 23) or low levels (33%, n = 13) of sphingomyelinase, which is reported to act synergistically with enterotoxins Nhe and Hbl. One strain isolated from rosemary was however classified as highly enterotoxic surpassing the cytotoxic activity of the high-level reference strain by a factor of 1.5. This strain also produced vast amounts of sphingomyelinase. Combining all results obtained in this study into a fingerprint pattern, several enterotoxic biopesticide strains were indistinguishable from those of isolates from foods or collected in association with outbreaks. Our study shows that many B. thuringiensis biopesticide strains exhibit mid-level cytotoxicity in a Vero cell assay and that some of these strains cannot be differentiated from isolates collected from foods or in association with outbreaks. Thus, we demonstrate that the use of B. thuringiensis strains as biopesticides can represent a food safety risk, underpinning the importance of assessing the hazardous potential of each strain and formulation used.

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Common occurrence of enterotoxin genes and enterotoxicity inBacillus thuringiensis

Cited by 101 publications

References 32 publications

Genetic and genomic diversity of NheABC locus from Bacillus strains

Genetic and genomic diversity of NheABC locus from Bacillus strains

Massive horizontal gene transfer, strictly vertical inheritance and ancient duplications differentially shape the evolution of Bacillus cereus enterotoxin operons hbl, cytK and nhe

Enterotoxin Production of Bacillus thuringiensis Isolates From Biopesticides, Foods, and Outbreaks

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