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Cereulide

Cereulide is a highly stable, cyclic dodecadepsipeptide toxin produced by emetic strains of the Gram-positive, spore-forming bacterium Bacillus cereus, serving as the primary causative agent of the emetic type of B. cereus foodborne illness. This pre-formed toxin, typically generated in contaminated starchy foods such as rice or pasta during improper storage, induces rapid-onset vomiting (0.5–5 hours post-ingestion) due to its role as a potassium ionophore that disrupts mitochondrial function and cellular energy production. Structurally, cereulide consists of three repeating units of the tetradepsipeptide sequence [D-O-Leu–D-Ala–L-O-Val–L-Val], forming a 36-membered ring with a molecular weight of approximately 1,153 , which confers its exceptional resistance to heat (surviving 121°C for 2 hours), extreme (2–12), and proteolytic degradation. It is biosynthesized via a non-ribosomal synthetase (NRPS) encoded by the ces operon, located on a 270 kb megaplasmid (pCER270) in producing strains, with optimal production occurring at temperatures between 12–37°C, neutral (6–7), and high (>0.953). The toxin's cytotoxicity primarily targets mitochondria by facilitating potassium influx, leading to uncoupling of , depletion of ATP, and subsequent , particularly in hepatic and pancreatic tissues. In humans, the estimated emetic dose ranges from 0.02–1.83 µg/kg body weight, though severe cases can result in , acute encephalopathy, or multi-organ dysfunction, with higher risks to children and the elderly. Unlike the diarrheal toxins of B. cereus, cereulide is not neutralized by and persists through cooking, underscoring the importance of rapid food to prevent its accumulation. Detection methods, such as (e.g., MALDI-TOF MS targeting m/z 1,175 or 1,191), enable quantification in food products at low levels (limit of detection ~30 pg/mL), aiding in outbreak investigations.

Chemical Properties

Structure

Cereulide is a cyclic dodecadepsipeptide toxin, consisting of a 36-membered ring formed by three repeating units of the tetrapeptide sequence D-O-Leu–D-Ala–L-O-Val–L-Val, where O-Leu and O-Val denote α-hydroxy acid derivatives of leucine and valine, respectively. This structure features alternating ester and amide bonds, with the esters linking the carboxylic acid of an amino acid residue to the hydroxyl group of the adjacent hydroxy acid, and the amides connecting the amino group of an amino acid to the carboxylic acid of the previous residue. The molecular formula of cereulide is C57H96N6O18, with a molecular weight of 1153 Da. The specific stereochemistry of cereulide includes D-configurations at the O-Leu and residues and L-configurations at the O-Val and Val residues within each repeating unit, contributing to its overall chiral architecture. This arrangement creates a rigid, bracelet-like cyclic structure that resembles the valinomycin, enabling selective binding of ions such as K+ and Rb+. The ring can be represented textually as:
cyclo[(D-O-Leu–D-Ala–L-O-Val–L-Val)<sub>3</sub>]
In this conformation, the complexation sites are primarily the six carbonyl oxygen atoms—three from the L-Val residues forming one coordination and three from the D-Ala residues forming the opposite —positioning the metal centrally within the through ion-dipole interactions.

Physical and Chemical Stability

Cereulide demonstrates exceptional thermal stability, remaining intact after exposure to 121°C for 90 minutes, which exceeds standard autoclaving conditions used in . This resistance persists even under alkaline conditions, such as pH 10.6, highlighting its robustness against high-temperature treatments. Due to its cyclic depsipeptide structure, which lacks free amino or carboxyl termini, cereulide is highly resistant to degradation by proteolytic enzymes like and . It also withstands extreme environments, maintaining stability across a range from pH 2 to 12, thereby surviving gastric passage and food acidification processes. As a lipophilic molecule, cereulide exhibits high solubility in organic solvents such as and , facilitating its extraction and analysis, while showing poor in , which limits its in aqueous food components. This property contributes to its accumulation in lipid-rich food matrices. In food systems, cereulide's stability ensures it persists through cooking, reheating, and prolonged storage, even at temperatures, posing a persistent as preformed evades common inactivation methods. For instance, it remains active in contaminated or dishes after or heating, underscoring the need for preventive measures targeting production rather than post-contamination remediation.

Biological Production

Producing Organism

is a Gram-positive, spore-forming, rod-shaped bacterium that is ubiquitous in natural environments, including , dust, vegetation, and various food matrices. As an opportunistic , it can contaminate raw materials and processed foods during production, persisting through sporulation under adverse conditions. Only specific emetic strains within the B. cereus group produce cereulide, distinguishing them from diarrheal strains that generate enterotoxins in the host intestine. These toxigenic emetic strains carry the , a genetic cluster located on a large (such as pCER270), which enables cereulide synthesis and is absent in non-emetic variants. Cereulide production occurs via a synthetase mechanism encoded by this operon. Cereulide formation is favored under aerobic conditions at temperatures between 22°C and 37°C, with optima varying from 24–30°C depending on strain and medium, such as in carbohydrate-rich media like or . The bacterium grows mesophilically from 10°C to 48°C but requires oxygen for toxin elaboration, showing reduced yields in settings. Emetic B. cereus strains are prevalent in contaminated foods like reheated (where up to 42% of isolates produce detectable cereulide), dairy products (prevalence of 4.8–56%), and (around 5%). Outbreaks often trace to improper storage of starchy or proteinaceous items, allowing and accumulation.

Biosynthesis Pathway

Cereulide is synthesized through a synthetase (NRPS) mechanism encoded by the , a located on a large related to pXO1 in emetic strains of . The operon consists of seven genes: cesH (encoding a putative ), cesP (phosphopantetheinyl transferase for NRPS activation), cesT (type II thioesterase for editing misincorporated monomers), cesA and cesB (the core NRPS synthetases), and cesC and cesD ( components potentially involved in export). This modular system assembles the cyclic dodecadepsipeptide cereulide, (D-O-Leu-D-Ala-L-O-Val-L-Val)3, without ribosomal involvement. The is driven by the multidomain enzymes CesA and CesB, which together form a tetramodular NRPS complex. CesA (approximately 10 kb) contains two modules with domains arranged as A-T-C-A-T-E-C, where A denotes adenylation (for substrate activation), T is peptidyl carrier protein (thiolation for loading), C is (for bond formation), and E is epimerization (for inversion). CesB (approximately 8 kb) comprises two additional modules in A-T-C-A-T-TE , with the C-terminal thioesterase (TE) domain responsible for release and cyclization. CesP activates the apo-NRPS by transferring a phosphopantetheine arm to the T domains, enabling substrate tethering, while CesT removes aberrant intermediates to ensure fidelity. The assembly proceeds stepwise across the four modules. In the first module of CesA, the A domain activates D-hydroxyisocaproic acid (derived from ) to form D-O-Leu, which is loaded onto the T domain; the subsequent C domain then facilitates ester bond formation with the incoming D-alanine (activated in the second A domain of CesA, with epimerization to D-Ala). The growing chain transfers to the first module of CesB, where L-hydroxyisovaleric acid (from ) is activated as L-O-Val and linked via bond by the C domain. The final module activates and incorporates L-valine through formation. This unit (D-O-Leu-D-Ala-L-O-Val-L-Val) is repeated three times through iterative use of the four modules in the CesA-CesB complex, yielding a linear dodecadepsipeptide; the TE domain then catalyzes macrocyclization by nucleophilic attack and of the , releasing the cyclic product. Expression of the ces is tightly regulated by promoter elements and environmental cues. The primary promoter P1, located upstream of cesP, drives transcription of the polycistronic cesPTABCD mRNA, while a separate promoter controls cesH; weaker internal promoters near cesB and cesT contribute minimally. Transcription is positively regulated by Spo0A (a sporulation master regulator) and repressed by AbrB during early , with CodY further inhibiting expression under nutrient-rich conditions. Optimal production occurs at temperatures between 22°C and 37°C in carbohydrate-rich media, such as those mimicking cooked rice, where elevated temperatures (above 30°C) or protein-dominated environments suppress ces expression, linking synthesis to sporulation cues and food matrix conditions.

Toxicity and Health Effects

Mechanism of Action

Cereulide exerts its toxicity primarily through mitochondrial disruption, functioning as a highly selective (K⁺) ionophore that facilitates the transport of K⁺ ions across membranes. This ionophoric activity leads to the collapse of the by promoting K⁺ influx into the , resulting in membrane depolarization and swelling. Consequently, cereulide uncouples from electron transport, severely impairing the proton motive force required for ATP production. The inhibition of ATP synthesis by cereulide is particularly pronounced in metabolically active cells, such as those in the liver (HepG2 cells) and intestines ( cells), where exposure leads to a drastic reduction in ATP levels—for instance, dropping to approximately 6% of control values in HepG2 cells at concentrations as low as 0.5 nM. This energy depletion triggers cellular stress responses, culminating in or , with liver cells exhibiting degeneration and while intestinal cells show barrier dysfunction and . The toxin's lipophilic nature, stemming from its cyclic depsipeptide , allows it to readily partition into and bind non-covalently to mitochondrial membranes without forming permanent chemical bonds, enhancing its ability to insert and form channels. Toxicity manifests in a dose-dependent manner, with acute effects observed in animal models; for example, the (LD50) in mice via ranges from approximately 100 to 600 μg/kg body weight, reflecting the rapid onset of mitochondrial failure leading to .

Clinical Symptoms and Outbreaks

Cereulide intoxication primarily manifests as the emetic syndrome, with symptoms including , , and abdominal cramps appearing 1 to 5 hours after ingestion of contaminated . These symptoms typically last 8 to 10 hours and are usually self-limiting, though may persist. In severe cases, cereulide exposure can lead to , , and death, particularly at higher doses. Fatalities have been documented in pediatric cases, with an estimated emetic toxic dose of approximately 8 μg/kg body weight. Notable outbreaks include a 2003 incident in involving a family of five children who consumed B. cereus-contaminated ; all developed emetic symptoms, and one 7-year-old girl died from acute hepatic . Another significant case occurred in in 2008, where three family members experienced after eating reheated ; the 1-year-old boy succumbed to acute hepatic within 6 hours, while the others recovered. A more recent emetic outbreak linked to cereulide occurred in 2021 in , affecting over 100 schoolchildren who consumed contaminated , presenting with and within 0.5–4.5 hours. Commercial infant formulas have been identified as a risk for cereulide production by B. cereus, with studies isolating toxigenic strains from products in and demonstrating high yields in cereal-dairy mixtures, contributing to emetic episodes in s. Children and immunocompromised individuals are particularly susceptible due to lower body mass, immature pathways, and heightened vulnerability to organ damage.

Detection and Prevention

Analytical Methods

Liquid chromatography-tandem (LC-MS/MS) serves as the gold standard for the detection and quantification of cereulide in samples due to its high , specificity, and ability to handle complex matrices. This method involves in positive mode, monitoring the precursor ion at m/z 1170.7 and product ions at m/z 314.2 and 499.3, with limits of detection () as low as 0.1 ng/g and limits of quantification (LOQ) around 0.5–1 ng/g in foods like and . Validation studies confirm (R² > 0.99), rates of 70–120%, and with relative deviations below 10%, making it suitable for regulatory monitoring. Bioassays provide a functional approach to detect cereulide by assessing its mitochondrial , with the MTT using mammalian cell lines such as HEp-2 being a common screening tool. In this , cereulide induces dose-dependent through mitochondrial dysfunction, measured by reduced production after 24–48 hours of exposure, with sensitivity detecting as low as 1–10 ng/mL. The method is semi-quantitative and complements instrumental techniques by confirming , though it may be affected by matrix interferences from food extracts. Immunoassays, such as enzyme-linked immunosorbent assays (), target the cyclic depsipeptide structure of cereulide but are rarely used due to challenges in development for this small, non-immunogenic . While prototypes exist, no widely available commercial kits are established, limiting their application for precise quantification. is critical for all methods, particularly for complex matrices like , where cereulide extraction typically involves or to achieve high recovery (>80%). For a 3 g sample, 15 mL of is added, followed by vortex mixing, shaking for 15 minutes, and centrifugation at 4000 × g; the supernatant is then diluted and filtered before analysis to remove and particulates. Cleanup steps, such as , enhance purity for LC-MS/MS, ensuring accurate results in starchy foods.

Food Safety Measures

To mitigate the risks of cereulide contamination, food safety measures emphasize preventing the growth of Bacillus cereus and the subsequent production of the heat-stable emetic , as cereulide once formed cannot be reliably inactivated by standard cooking or reheating processes. Cooking guidelines recommend thorough initial cooking of starchy foods like and to at least 63°C (145°F) to reduce vegetative cells, followed by rapid cooling to below 4°C within two hours to inhibit and synthesis; reheating such foods multiple times should be avoided, as it does not degrade pre-formed cereulide and may promote bacterial proliferation if temperatures are not maintained above 60°C. Regulatory frameworks, such as those from the (EFSA), establish process hygiene criteria for B. cereus in vulnerable products like infant formulae, targeting presumptive counts below 10^5 CFU/g to minimize emetic risks, while an estimated toxic dose of cereulide at or above 8 μg/kg body weight is associated with acute illness, guiding exposure assessments rather than strict residue limits. and Critical Control Points (HACCP) plans are mandated for food production to control B. cereus by identifying critical points like cooling and storage, ensuring temperatures remain either above 60°C or below 4°C to prevent sporulation and production in high-risk items such as ready-to-eat cereals and . In industrial settings, interventions prioritize contamination prevention over post-production treatments, as (e.g., 72°C for 15 seconds) fails to eliminate B. cereus spores or degrade cereulide due to their thermal stability, shifting focus to sourcing, rapid chilling post-processing, and to limit sporulation in and starchy product lines. For consumers, practical advice includes discarding foods left at for over two hours, especially reheated , , or products showing signs of spoilage like off odors or sliminess, and routinely checking high-risk items such as powdered or soft cheeses for proper to avoid B. cereus growth.

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