Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains.

An in-depth polyphasic approach was applied to study the population structure of the human pathogen Bacillus cereus. To assess the intraspecific biodiversity of this species, which is the causative agent of gastrointestinal diseases, a total of 90 isolates from diverse geographical origin were studied by genetic [M13-PCR, random amplification of polymorphic DNA (RAPD), multilocus sequence typing (MLST)] and phenetic [Fourier transform Infrared (FTIR), protein profiling, biochemical assays] methods. The strain set included clinical strains, isolates from food remnants connected to outbreaks, as well as isolates from diverse food environments with a well documented strain history. The phenotypic and genotypic analysis of the compiled panel of strains illustrated a considerable diversity among B. cereus connected to diarrhoeal syndrome and other non-emetic food strains, but a very low diversity among emetic isolates. Using all typing methods, cluster analysis revealed a single, distinct cluster of emetic B. cereus strains. The isolates belonging to this cluster were neither able to degrade starch nor could they ferment salicin; they did not possess the genes encoding haemolysin BL (Hbl) and showed only weak or no haemolysis. In contrast, haemolytic-enterotoxin-producing B. cereus strains showed a high degree of heterogeneity and were scattered over different clusters when different typing methods were applied. These data provide evidence for a clonal population structure of cereulide-producing emetic B. cereus and indicate that emetic strains represent a highly clonal complex within a potentially panmictic or weakly clonal background population structure of the species. It may have originated only recently through acquisition of specific virulence factors such as the cereulide synthetase gene.

[1]  M. Andersson,et al.  Identification and Partial Characterization of the Nonribosomal Peptide Synthetase Gene Responsible for Cereulide Production in Emetic Bacillus cereus , 2005, Applied and Environmental Microbiology.

[2]  M. Kimura A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences , 1980, Journal of Molecular Evolution.

[3]  S. Scherer,et al.  Bacillus cereus, the causative agent of an emetic type of food-borne illness. , 2004, Molecular nutrition & food research.

[4]  E. Holmes,et al.  Population Structure and Evolution of the Bacillus cereus Group , 2004, Journal of bacteriology.

[5]  David A Rasko,et al.  Identification of anthrax toxin genes in a Bacillus cereus associated with an illness resembling inhalation anthrax. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Siegfried Scherer,et al.  Identification of emetic toxin producing Bacillus cereus strains by a novel molecular assay. , 2004, FEMS microbiology letters.

[7]  Anne-Brit Kolstø,et al.  Fluorescent Amplified Fragment Length Polymorphism Analysis of Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis Isolates , 2004, Applied and Environmental Microbiology.

[8]  Nicolas J. Tourasse,et al.  Multilocus Sequence Typing Scheme for Bacteria of the Bacillus cereus Group , 2004, Applied and Environmental Microbiology.

[9]  S. Scherer,et al.  Temporal Stability and Biodiversity of Two Complex Antilisterial Cheese-Ripening Microbial Consortia , 2003, Applied and Environmental Microbiology.

[10]  M. Salkinoja-Salonen,et al.  Potential of Bacillus cereus for producing an emetic toxin, cereulide, in bakery products: quantitative analysis by chemical and biological methods. , 2003, Journal of food protection.

[11]  B. Spratt,et al.  How Clonal Is Staphylococcus aureus? , 2003, Journal of bacteriology.

[12]  P. E. Granum,et al.  Pathogenic potential of fifty Bacillus weihenstephanensis strains. , 2002, FEMS microbiology letters.

[13]  R. Mikkola,et al.  Inhibition of human natural killer cell activity by cereulide, an emetic toxin from Bacillus cereus , 2002, Clinical and experimental immunology.

[14]  Christophe Nguyen-The,et al.  Enterotoxigenic Profiles of Food-Poisoning and Food-Borne Bacillus cereus Strains , 2002, Journal of Clinical Microbiology.

[15]  Joachim Charzinski,et al.  Intraspecific diversity of Brevibacterium linens, Corynebacterium glutamicum and Rhodococcus erythropolis based on partial 16S rDNA sequence analysis and Fourier-transform infrared (FT-IR) spectroscopy. , 2002, Microbiology.

[16]  Denis Bourguet,et al.  Genetic Differentiation between Sympatric Populations of Bacillus cereus and Bacillus thuringiensis , 2002, Applied and Environmental Microbiology.

[17]  Siegfried Scherer,et al.  Identification of coryneform bacteria and related taxa by Fourier-transform infrared (FT-IR) spectroscopy. , 2002, International journal of systematic and evolutionary microbiology.

[18]  G. Baranton,et al.  The implications of a low rate of horizontal transfer in Borrelia. , 2001, Trends in microbiology.

[19]  B. Spratt,et al.  Recombination and the population structures of bacterial pathogens. , 2001, Annual review of microbiology.

[20]  E. Feil,et al.  Population structure and evolutionary dynamics of pathogenic bacteria , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[21]  P. E. Granum,et al.  A new cytotoxin from Bacillus cereus that may cause necrotic enteritis , 2000, Molecular microbiology.

[22]  Anne-Brit Kolstø,et al.  Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis—One Species on the Basis of Genetic Evidence , 2000, Applied and Environmental Microbiology.

[23]  B. Cookson,et al.  Fluorescent amplified-fragment length polymorphism analysis of the MRSA epidemic. , 2000, FEMS microbiology letters.

[24]  E. Stackebrandt,et al.  Cultivatable microbial biodiversity: gnawing at the Gordian knot. , 2000, Environmental microbiology.

[25]  A. Kolstø,et al.  Genetic Structure of Population of Bacillus cereus and B. thuringiensis Isolates Associated with Periodontitis and Other Human Infections , 2000, Journal of Clinical Microbiology.

[26]  S. Scherer,et al.  The Hemolytic Enterotoxin HBL Is Broadly Distributed among Species of the Bacillus cereusGroup , 1999, Applied and Environmental Microbiology.

[27]  P. E. Granum,et al.  The sequence of the non-haemolytic enterotoxin operon from Bacillus cereus. , 1999, FEMS microbiology letters.

[28]  L. Price,et al.  Genetic Diversity in the Protective Antigen Gene ofBacillus anthracis , 1999, Journal of bacteriology.

[29]  N. A. Logan,et al.  Semiautomated Metabolic Staining Assay for Bacillus cereus Emetic Toxin , 1999, Applied and Environmental Microbiology.

[30]  M. Salkinoja-Salonen,et al.  Evaluation of methods for recognising strains of the Bacillus cereus group with food poisoning potential among industrial and environmental contaminants. , 1999, Systematic and applied microbiology.

[31]  C. Sorlini,et al.  A Randomly Amplified Polymorphic DNA Marker Specific for the Bacillus cereus Group Is Diagnostic forBacillus anthracis , 1999, Applied and Environmental Microbiology.

[32]  J. M. Smith,et al.  Free recombination within Helicobacter pylori. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[33]  S. Scherer,et al.  Bacillus weihenstephanensis sp. nov. is a new psychrotolerant species of the Bacillus cereus group. , 1998, International journal of systematic bacteriology.

[34]  B. Svensson,et al.  A RAPD‐PCR method for large‐scale typing of Bacillus cereus , 1998, Letters in applied microbiology.

[35]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[36]  Yves Van de Peer,et al.  Construction of evolutionary distance trees with TREECON for Windows: accounting for variation in nucleotide substitution rate among sites , 1997, Comput. Appl. Biosci..

[37]  S. Krähenbühl,et al.  Fulminant liver failure in association with the emetic toxin of Bacillus cereus. , 1997, The New England journal of medicine.

[38]  A G Williams,et al.  Effect of sampling procedure and strain variation in Listeria monocytogenes on the discrimination of species in the genus Listeria by Fourier transform infrared spectroscopy and canonical variates analysis. , 1997, FEMS microbiology letters.

[39]  M Hugh-Jones,et al.  Molecular evolution and diversity in Bacillus anthracis as detected by amplified fragment length polymorphism markers , 1997, Journal of bacteriology.

[40]  Willem,et al.  On the nature and use of randomly amplified DNA from Staphylococcus aureus , 1996, Journal of clinical microbiology.

[41]  V. Stanisich,et al.  New approaches to typing and identification of bacteria using the 16S-23S rDNA spacer region. , 1996, Microbiology.

[42]  J. L. Schoeni,et al.  Bacillus cereus . Enterotoxic activity of hemolysin BL from , 1995 .

[43]  H. Konuma,et al.  Emesis of rhesus monkeys induced by intragastric administration with the HEp-2 vacuolation factor (cereulide) produced by Bacillus cereus. , 1995, FEMS microbiology letters.

[44]  M. Mori,et al.  A novel dodecadepsipeptide, cereulide, isolated from Bacillus cereus causes vacuole formation in HEp-2 cells. , 1994, FEMS microbiology letters.

[45]  P. E. Granum Bacillus cereus and its toxins. , 1994, Society for Applied Bacteriology symposium series.

[46]  C. J. Duggleby,et al.  Differentiation of Bacillus anthracis from other Bacillus cereus group bacteria with the PCR. , 1994, International journal of systematic bacteriology.

[47]  J. Heinrichs,et al.  Molecular cloning and characterization of the hblA gene encoding the B component of hemolysin BL from Bacillus cereus , 1993, Journal of bacteriology.

[48]  F. Drobniewski,et al.  Bacillus cereus and related species , 1993, Clinical Microbiology Reviews.

[49]  D. Dykhuizen,et al.  Recombination in Escherichia coli and the definition of biological species , 1991, Journal of bacteriology.

[50]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[51]  F. Priest,et al.  A frequency matrix for probabilistic identification of some bacilli. , 1988, Journal of general microbiology.

[52]  F. Priest,et al.  A numerical classification of the genus Bacillus. , 1988, Journal of general microbiology.

[53]  D. Claus,et al.  Genus Bacillus Cohn 1872, 174^ , 1986 .

[54]  Dm Jones A Colour Atlas of Bacillus Species , 1983 .

[55]  W. Haynes,et al.  The genus Bacillus , 1973 .

[56]  J. H. Ward Hierarchical Grouping to Optimize an Objective Function , 1963 .