Environment driven cereulide production by emetic strains of Bacillus cereus

Apetroaie-Constantin, Camelia; Shaheen, Ranad; Andrup, Lars; Smidt, Lasse; Rita, Hannu; Salkinoja‐Salonen, Mirja

doi:10.1016/j.ijfoodmicro.2008.06.006

Cited by 30 publications

(14 citation statements)

References 54 publications

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“…We recently showed that B. cereus benefits from its produced cereulide in a potassium-deficient environment (Ͻ1 mM) but not in potassium-rich environment (36). This may explain why potato endophytic B. cereus were frequently cereulide producers, similarly to what was earlier observed for endophytic B. cereus from Norway spruce (Picea abies), where four of the six B. cereus isolates were cereulide producers (NS58, NS88, NS115, and NS117 [20,36,50,51]). …”

Section: Discussionsupporting

confidence: 58%

“…Endophytic cereulide-producing B. cereus organisms from spruce (Picea abies) were also reported to differ in ribopatterns from the nonproducers (NS61 and NS88 [20]). The potato isolates differed from the spruce tree producers in ribopatterns and modest cereulide production, 1 to 100 ng mg of biomass Ϫ1 compared 900 to 1,700 ng mg of biomass Ϫ1 for the NS strains (Norway spruce [51,52,54]). It might be that each plant species carries its own B. cereus cereulide-producing genotype, possibly adapted to the specific metabolic environment inside the host plant.…”

Section: Discussionmentioning

confidence: 97%

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Potato Crop as a Source of Emetic Bacillus cereus and Cereulide-Induced Mammalian Cell Toxicity

Hoornstra

Andersson

Теплова

et al. 2013

Appl Environ Microbiol

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e Bacillus cereus, aseptically isolated from potato tubers, were screened for cereulide production and for toxicity on human and other mammalian cells. The cereulide-producing isolates grew slowly, the colonies remained small (ϳ1 mm), tested negative for starch hydrolysis, and varied in productivity from 1 to 100 ng of cereulide mg (wet weight) ؊1 (ϳ0.01 to 1 ng per 10 5 CFU). By DNA-fingerprint analysis, the isolates matched B. cereus F5881/94, connected to human food-borne illness, but were distinct from cereulide-producing endophytes of spruce tree (Picea abies). Exposure to cell extracts (1 to 10 g of bacterial biomass ml ؊1 ) and to purified cereulide (0.4 to 7 ng ml ؊1 ) from the potato isolates caused mitochondrial depolarization (loss of ⌬⌿m) in human peripheral blood mononuclear cells (PBMC) and keratinocytes (HaCaT), porcine spermatozoa and kidney tubular epithelial cells (PK-15), murine fibroblasts (L-929), and pancreatic insulin-producing cells (MIN-6). Cereulide (10 to 20 ng ml ؊1 ) exposed pancreatic islets (MIN-6) disintegrated into small pyknotic cells, followed by necrotic death. Necrotic death in other test cells was observed only after a 2-log-higher exposure. Exposure to 30 to 60 ng of cereulide ml ؊1 induced K ؉ translocation in intact, live PBMC, keratinocytes, and sperm cells within seconds of exposure, depleting 2 to 10% of the cellular K ؉ stores within 10 min. The ability of cereulide to transfer K ؉ ions across biological membranes may benefit the producer bacterium in K ؉ -deficient environments such as extracellular spaces inside plant tissue but is a pathogenic trait when in contact with mammalian cells. C ereulide, the emetic toxin of Bacillus cereus, is most likely responsible for the severe cases of illness connected to the consumption of food contaminated with B. cereus (1-9). Cereulideproducing B. cereus isolates are frequently reported in processed foods, implicated (3-16) or not implicated (17-21) with foodborne illness, but appear infrequently in farming or natural outdoor environments (22-26).B. cereus is known to occur in the rhizomicrobiota and endophytic community of plants, as well as in root vegetables, including potato (27), but these habitats have not been searched for cereulide producers (28). The extracellular spaces of plants, as well as natural waters, including soil water, contain Ͻ1 mM K ϩ ions, whereas the concentration of K ϩ in the interior of the cytoplasmic space of plant cells, as well as in bacteria, is Ͼ100 mM (29, 30). Bacteria living in the extracellular spaces of the tuber of a crop plant must thus compete for K ϩ ions with its plant host and with other bacteria inside the crop plant.Cereulide is known to be a heat-stable cyclic depsipeptide (6, 31, 32) with high affinity and selectivity for sequestering K ϩ ions from a low-potassium environment (33-35). We recently found (36) that an endophytic, cereulide-producing Bacillus cereus strain (37) from Picea abies (Norway spruce), had a competitive advantage against nonproducers in potassium-deficient (Ͻ...

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Section: Discussionsupporting

confidence: 58%

Section: Discussionmentioning

confidence: 97%

Potato Crop as a Source of Emetic Bacillus cereus and Cereulide-Induced Mammalian Cell Toxicity

Hoornstra

Andersson

Теплова

et al. 2013

Appl Environ Microbiol

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show abstract

“…The fingerprinting of whole-cell DNA by ribopattern analysis was done as described previously by Apetroaie-Constantin et al (5), with EcoRI restriction using an automated ribotyper (RiboPrinter microbial characterization system; DuPont Qualicon, Wilmington, DE) and RiboExplorer software, version 2.1.4216.0. The Bacillus cereus-targeted PCR assay using whole-cell DNA and primers S-S-Bc-200-a-S-18 and S-S-Bc-470-a-A-18 was conducted as described previously by Hansen et al (25).…”

Section: Or 50 G Of Nacl Litermentioning

confidence: 99%

Psychrotolerant Paenibacillus tundrae Isolates from Barley Grains Produce New Cereulide-Like Depsipeptides (Paenilide and Homopaenilide) That Are Highly Toxic to Mammalian Cells

Rasimus

Mikkola

Andersson

et al. 2012

Appl Environ Microbiol

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“…, equivalent to a cellular cereulide concentration of 500-1500 mM (Apetroaie et al, 2005;Apetroaie-Constantin et al, 2008). This method of generating DY could serve as a temporary mechanism to energize vital transport functions such as the import of organic substrates for subsequent generation of proton motive force.…”

mentioning

confidence: 99%

Cereulide produced by Bacillus cereus increases the fitness of the producer organism in low-potassium environments

et al. 2012

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Cereulide, produced by certain Bacillus cereus strains, is a lipophilic cyclic peptide of 1152 Da that binds K + ions with high specificity and affinity. It is toxic to humans, but its role for the producer organism is not known. We report here that cereulide operates for B. cereus to scavenge potassium when the environment is growth limiting for this ion. Cereulide-producing B. cereus showed higher maximal growth rates (m max ) than cereulide non-producing B. cereus in K + -deficient medium (K + concentration~1 mM). The cereulide-producing strains grew faster in K + -deficient than in K + -rich medium with or without added cereulide. Cereulide non-producing B. cereus neither increased m max in K + -deficient medium compared with K + -rich medium, nor benefited from added cereulide.Cereulide-producing strains outcompeted GFP-labelled Bacillus thuringiensis in potassiumdeficient (K + concentration~1 mM) but not in potassium-rich (K + concentration~30 mM) medium. Exposure to 2 mM cereulide in potassium-free medium lacking an energy source caused, within seconds, a major efflux of cellular K + from B. cereus not producing cereulide as well as from Bacillus subtilis. Cereulide depleted the cereulide non-producing B. cereus and B. subtilis cells of a major part of their K + stores, but did not affect cereulide-producing B. cereus strains. Externally added 6-10 mM cereulide triggered the generation of biofilms and pellicles by B. cereus. The results indicate that both endogenous and externally accessible cereulide supports the fitness of cereulide-producing B. cereus in environments where the potassium concentration is low.

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Environment driven cereulide production by emetic strains of Bacillus cereus

Cited by 30 publications

References 54 publications

Potato Crop as a Source of Emetic Bacillus cereus and Cereulide-Induced Mammalian Cell Toxicity

Potato Crop as a Source of Emetic Bacillus cereus and Cereulide-Induced Mammalian Cell Toxicity

Psychrotolerant Paenibacillus tundrae Isolates from Barley Grains Produce New Cereulide-Like Depsipeptides (Paenilide and Homopaenilide) That Are Highly Toxic to Mammalian Cells

Cereulide produced by Bacillus cereus increases the fitness of the producer organism in low-potassium environments

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