Abstract
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.
Highlights
Bacillus cereus sensu lato comprises eight closely related species including the human pathogens Bacillus anthracis and Bacillus cereus
Some B. cereus sensu lato genomes seem to support this hypothesis of a reduced genome size in pathogens, such as B. anthracis (5.0 – 5.5 Mbp), B. cytotoxicus (4.1 Mbp) and some of the enteropathogenic strains we sequenced
Several exceptions like the enterotoxic non-hemolytic enterotoxin (Nhe) reference strain B. cereus NVH 0075–95 (6.1 Mbp) support the notion that genome size does not correlate with pathogenicity
Summary
Bacillus cereus sensu lato comprises eight closely related species including the human pathogens Bacillus anthracis and Bacillus cereus. B. cereus sensu stricto, which was discovered in 1887 as a bacterium occurring ubiquitously in nature [1], contains probiotic as well as pathogenic strains The latter are mostly associated with food-borne illness characterized by diarrhea or vomiting, but occasionally B. cereus is responsible for severe infections, e.g. endophthalmitis or meningitis [2]. In 1998, a highly enterotoxic and rare variant of cytotoxin K, CytK-1, was discovered in B. cereus NVH 391–98, a strain responsible for severe food poisoning This strain was published in 2013 as the type strain of the new species B. cytotoxicus on the basis of presence of the cytK-1 gene, its thermotolerance (growth at up to 50 °C), a distinctive fatty acid profile, DNA-DNA hybridization and multilocus sequence typing (MLST) [16]. B. toyonensis was distinguished from other B. cereus sensu lato type species by pairwise calculations of the average nucleotide identity (ANI)
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