Bacillus cereus spores present in soil (or faeces) are ingested by arthropods. In the moist- and nutrient-rich intestines of healthy soil arthropods, germination occurs, followed by motile and filamentous growth, attached to the chitinous intestinal epithelium, and finally resporulation in the distal unattached end of the filaments (Margulis et al., 1998). Similarly, B. cereus s. s., B. thuringiensis and B. mycoides/B. pseudomycoides have been isolated from the digestive tracts of terrestrial arthropods (sow bugs; Swiecicka & Mahillon, 2006). Defecation or natural death of the host releases the cells and/or spores again into the soil. This represents the symbiotic lifestyle of B. cereus, which can be either commensal or mutualistic, if there are no effects or beneficial effects for the arthropod host, respectively. Although no proof of mutual beneficial relations has been provided, it is plausible to assume that intestinal B. cereus aid in the nutrient digestion of their hosts, since B. cereus group strains produce extracellular enzymes to degrade complex organic materials in soil (Luo et al., 2007; Gao et al., 2008). Moreover, B. cereus can produce various toxins, bacteriocins and antibiotics in the competition with other microbiota, which could protect the arthropod host against enteric pathogens (Bizani et al., 2005; Tempelaars et al., 2011). However, the pathogenic life cycle is also observed in insects depending on the specific strain and insect, for example B. thuringiensis subsp. kurstaki in lepidopteran and dipteran insects (Sevim et al., 2012). In this case, B. cereus strains kill the host by intestinal toxin production, followed by colonization and multiplication in the cadaver and eventually resporulation and return to the soil as a spore (Swiecicka et al., 2008). Consequently, B. thuringiensis toxins have been widely applied as biological insecticides, thereby reducing the amount of chemicals required to control the major pests (Naranjo & Ellsworth, 2010). The most widely known and successful application consists of transgenic corn, producing B. thuringiensis (Bt) toxins against the European corn borer (Ostrinia nubilalis).
Similarly to the diverse relations with insects host, B. cereus strains can also live both their pathogenic and the symbiotic life cycle (commensalism or mutualism) in mammals. For example, the most notorious B. cereus group strains are undoubtedly B. anthracis strains, the causative agents of anthrax disease in livestock (Koch, 1878). Anthrax is a zoonosis which is contracted cutaneously, pulmonary or gastrointestinally from contaminated cattle, goat, sheep or soil, or by injection of contaminated illicit drugs (Ringertz et al., 2000; Mock & Fouet, 2001). In contrast, Bacillus cereus var. toyoi is a beneficial member of the intestinal microbiota, which leads to better feed conversion (Williams et al., 2009). These B. cereus spores are sold as a probiotic feed additive by Rubinum S.A. under the name Toyocerin®, which is authorized in the EU as feed additive for poultry, swine, bovines and rabbits by EFSA. This probiotic B. cereus strain functions as a stabilizer of the intestinal microbiota and inhibitor of enteric bacteria such as Salmonella, Escherichia coli and clostridia to improve the feed conversion and performance of the animals (website Rubinum S.A.). Daily administration of 107 to 109 spores per kg body weight to various animals (rabbits, pigs, chickens, turkeys and cattle for 8–78 weeks) and even to human volunteers (five healthy males for 8 days) was found to be safe (Williams et al., 2009). As a result of its saprophytic soil life cycle, B. cereus is found in water, vegetables and many other food ingredients, resulting in the contamination of a wide variety of finished food products (see 'Risk food products'). Ingestion of B. cereus by humans can lead to emetic or diarrhoeal food poisoning (Fig. 2; see 'Emetic and diarrhoeal food poisoning caused by B. cereus'). Few diarrhoeal food poisoning cases have been attributed to B. thuringiensis strains, but this may be underreporting due to difficulties in species differentiation (Jackson et al., 1995; te Giffel et al., 1997). Interestingly, the presence of human intestinal cells specifically induces spore germination, indicating that the human gut is a specific favourable environment for B. cereus, activating its growth (Andersson et al., 1998; Wijnands et al., 2007). After multiplication and possibly sporulation in the host's intestinal tract, B. cereus cells and/or spores are excreted with the vomit and/or faeces, eventually return to the soil and thus end their pathogenic life cycle. Sometimes, the food poisoning cases can even have a lethal outcome due to dehydration or liver and brain damages after translocation of cereulide to those tissues (Posfay-Barbe et al., 2008; Shiota et al., 2010). Alternatively, consumption of B. cereus provokes no gastrointestinal illness, which exemplifies its symbiotic life cycle. After consumption of nonpathogenic strains or low quantities of pathogenic ones, B. cereus is also a common component of the normal transient intestinal microbiota, illustrated by its frequent (in 14–43% of the cases) isolation from healthy people's faeces (Ghosh, 1978; Turnbull & Kramer, 1985). Nevertheless, nonpathogenic B. cereus strains are unwelcome contaminants in food products, since they cause spoilage and economical losses, for example in milk (De Jonghe et al., 2010). Particularly B. weihenstephanensis strains are regarded food spoilage strains, because these psychrotolerant bacteria are capable of growth at refrigerator temperatures ≤ 7 °C (Lechner et al., 1998; Baron et al., 2007). After excessive vegetative multiplication and/or resporulation of B. cereus in food products, these are lost for human consumption and discarded, which completes their saprophytic life cycle during food spoilage. Besides food-borne illness, B. anthracis, B. cereus and B. thuringiensis strains have significant pathogenic potential to cause nongastrointestinal diseases. Bacillus cereus has been described in lethal nosocomial infections of immunosuppressed patients through contaminated ventilation equipment, catheters or linen and towels (Hernandez et al., 1998; Bottone, 2010). Bacillus cereus is also known for postsurgical and posttraumatic open-wound infections such as gunshot wounds, injection drug abuse, ground-contracted open-wound fractures and severe war wounds. Moreover, primary cutaneous infections by B. cereus are also described, resulting in skin lesions which resemble B. anthracis skin infections. Finally, inhaled B. cereus spores can cause serious life-threatening pulmonary infections. Therefore, vegetative B. cereus cells can colonize the human body in various ways, but always using toxin production to damage or invade the host tissues, for example the intestinal epithelium (food poisoning), eye (endophthalmitis), brain (meningitis, meningoencephalitis, subarachnoid haemorrhage and brain abscesses) and blood (bacteremia). Bacillus cereus produces multiple toxins (Nhe, Hbl and CytK) with haemolytic and cytotoxic activity due to pore formation in the cell membrane during vegetative growth (Beecher et al., 1995; Hardy et al., 2001; Lindbäck et al., 2004; Fagerlund et al., 2008). Enterotoxin EntFM, haemolysins, phospholipases C and other degradative enzymes are not directly cytotoxic, but they contribute to the cytotoxic and haemolytic activity of B. cereus and its adhesion to epithelial cells (Wazny et al., 1990; Asano et al., 1997; Firth et al., 1997; Beecher et al., 2000; Luxananil et al., 2003; Tran et al., 2010), resulting in detachment of the host's epithelial cells, microvilli damage, membrane damage, decreased mitochondrial activity and cell lysis (Minnaard et al., 2001; Ramarao & Lereclus, 2006).