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BMC Evol Biol. 2015 Nov 10;15:246. doi: 10.1186/s12862-015-0529-4.

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

Author information

  • 1Lehrstuhl für Mikrobielle Ökologie, Zentralinstitut für Ernährungs-und Lebensmittelforschung (ZIEL), Technische Universität München, Weihenstephaner Berg 3, D-85350, Freising, Germany. marlies.boehm@wzw.tum.de.
  • 2Lehrstuhl für Mikrobielle Ökologie, Zentralinstitut für Ernährungs-und Lebensmittelforschung (ZIEL), Technische Universität München, Weihenstephaner Berg 3, D-85350, Freising, Germany. christopher.huptas@wzw.tum.de.
  • 3Lehrstuhl für Mikrobielle Ökologie, Zentralinstitut für Ernährungs-und Lebensmittelforschung (ZIEL), Technische Universität München, Weihenstephaner Berg 3, D-85350, Freising, Germany. vk@borreliosecentrum.de.
  • 4Current address: BCA-clinic Betriebs GmbH & Co. KG, Morellstr. 33, D-86159, Augsburg, Germany. vk@borreliosecentrum.de.
  • 5Lehrstuhl für Mikrobielle Ökologie, Zentralinstitut für Ernährungs-und Lebensmittelforschung (ZIEL), Technische Universität München, Weihenstephaner Berg 3, D-85350, Freising, Germany. siegfried.scherer@wzw.tum.de.

Abstract

BACKGROUND:

Bacillus 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.

RESULTS:

We 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 hbl a 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.

CONCLUSIONS:

Frequent 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.

PMID:
26555390
PMCID:
PMC4641410
DOI:
10.1186/s12862-015-0529-4
[PubMed - indexed for MEDLINE]
Free PMC Article
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