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Comparison of B. cereus Group Genomes: How Did Pathogenicity Evolve?

Genome sequencing efforts have additionally made available the genome sequences from two B. cereus strains that have not been described as being particularly pathogenic. Together these sequences offer a unique glimpse into the geno-mic organization of the B. cereus sensu lato group, their ecology, evolution, and on the determinants that provoke different levels of virulence especially when compared to the genome of B. anthracis. One of the studied genomes is from the type strain ATCC 14579, the other from a dairy isolate of B. cereus ATCC 10987 that is genetically close to B. anthracis and has several unique metabolic capabilities such as urease and xylose utilization.

The type strain of B. cereus ATCC 14579 has a genome size of 5.42 Mbp. Part of the genome is a linear plasmid of 15.1 kbp length, designated pBClin15. The genome of the dairy isolate B. cereus ATCC 10987 that was isolated from a cheese spoilage in Canada in 1930 is very similar to this, with a genome size of 5.2 Mbp [85] and a 208-kbp plasmid pBc10987 that codes for 242 genes. Comparison of pBc10987 to pXO1 from B. anthracis revealed that around 65% of the proteins where homologous, and approximately 50% were in a syntenic location, showing a clear relationship between the two plasmids. An important difference from pXO1 from B. anthracis is that the pathogenicity island containing the genes for the regulator AtxA, the protective antigen, and the edema factor is absent from pBC10987. This region has been replaced on pBc10987 by genes for a copper-requiring tyrosinase, amino acid transport systems, an arsenate resistance cluster, and regulatory proteins. In addition, pBc10987 includes an MIP family channel protein and a possible metalloprotease, which are two new potential virulence factors.

There is a large core set that includes 75-80% of the genes sharing 80-100% amino acid identity with orthologous genes in B. anthracis. What is remarkable for reputedly non pathogenic strains is that this core set includes numerous factors for invasion, establishment, and propagation of bacteria within the host. B. cereus ATCC 14579 includes all but two toxins ever identified in clinical B. cereus isolates. B. cereus ATCC 10987 was already known to contain phosphatidylinositol-specific and phosphatidylcholine-preferring phospholipases C, sphingomyelinase, non-hemolytic enterotoxin, and proteases [86, 87]. It is interesting that this common set also comprises genes that can be attributed to insect pathogenesis. Examples are the three homologues of the immune inhibitor A protein (InhA), which selectively cleaves insect antibacterial peptides [73], or the presence of a homologue to the metalloprotease enhancin that confers the ability to cleave the intestinal mucin [72].

Common to all genomes seems to be the presence of the PlcR regulon that includes a number of virulence factors in B. cereus and B. anthracis despite the fact that PlcR is truncated in B. anthracis. There are 52 putative PlcR-binding sites that have been predicted in silico in the B. anthracis genome, 56 in B. cereus ATCC 14579, and 57 in B. cereus ATCC 10987.

Approximately 15% of the open reading frames found in B. cereus have no similarity to genes present in B. anthracis. For instance, chromosomal clusters of up to 20 kbp in length that code for capsular polysaccharide biosynthesis, including genes for glycosyltransferases, translocases, and a polysaccharide polymerization machinery, are specific for each B. cereus sequence and are absent from B. anthracis.

The presence of genes coding for potential pathogenicity factors in the core genome of B. cereus, B. anthracis, and B. thuringiensis is consistent with the view that the ancestor of the B. cereus group was an opportunistic insect pathogen rather than a benign soil bacterium [88].

Acknowledgement

The authors wish to thank their colleagues in the lab who contributed to the experimental work connected with their review. The work was supported by grants of the Niedersächsisches Ministerium für Wissenschaft und Kultur to the Göttingen Genomics Laboratory and of the Bundesministerium für Bildung und Forschung to the BiotechGenoMik network Göttingen.

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