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Comparative Study
. 2009 Oct 20;106(42):17939-44.
doi: 10.1073/pnas.0903585106. Epub 2009 Oct 6.

Comparative Genomics Reveal the Mechanism of the Parallel Evolution of O157 and non-O157 Enterohemorrhagic Escherichia Coli

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Free PMC article
Comparative Study

Comparative Genomics Reveal the Mechanism of the Parallel Evolution of O157 and non-O157 Enterohemorrhagic Escherichia Coli

Yoshitoshi Ogura et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

Among the various pathogenic Escherichia coli strains, enterohemorrhagic E. coli (EHEC) is the most devastating. Although serotype O157:H7 strains are the most prevalent, strains of different serotypes also possess similar pathogenic potential. Here, we present the results of a genomic comparison between EHECs of serotype O157, O26, O111, and O103, as well as 21 other, fully sequenced E. coli/Shigella strains. All EHECs have much larger genomes (5.5-5.9 Mb) than the other strains and contain surprisingly large numbers of prophages and integrative elements (IEs). The gene contents of the 4 EHECs do not follow the phylogenetic relationships of the strains, and they share virulence genes for Shiga toxins and many other factors. We found many lambdoid phages, IEs, and virulence plasmids that carry the same or similar virulence genes but have distinct evolutionary histories, indicating that independent acquisition of these mobile genetic elements has driven the evolution of each EHEC. Particularly interesting is the evolution of the type III secretion system (T3SS). We found that the T3SS of EHECs is composed of genes that were introduced by 3 different types of genetic elements: an IE referred to as the locus of enterocyte effacement, which encodes a central part of the T3SS; SpLE3-like IEs; and lambdoid phages carrying numerous T3SS effector genes and other T3SS-related genes. Our data demonstrate how E. coli strains of different phylogenies can independently evolve into EHECs, providing unique insights into the mechanisms underlying the parallel evolution of complex virulence systems in bacteria.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Circular maps of the O26, O111, and O103 chromosomes. From the outside in: (First circle) nucleotide sequence positions (in Mb); (Second and Third circles) CDSs transcribed clockwise and counterclockwise, respectively; (Fourth circle) locations of PPs and IEs: (red) lambdoid PPs; (purple) other PPs; (yellow) IEs; (Fifth circle) G+C content; (Sixth to Fourteenth circle) CDSs conserved in O157, O26, O111, O103, CFT073, E24377A, Sb227, Sd197, and K-12 MG1655, respectively.
Fig. 2.
Fig. 2.
Chromosomal integration sites of PPs and IEs found in the 7 fully sequenced E. coli strains (O157 Sakai, O26, O111, O103, K-12 MG1655, SE11, and E2348/69) are shown schematically. Only the strains in which PPs and IEs have been fully annotated were used in the analysis.
Fig. 3.
Fig. 3.
Genome-wide phylogenetic analysis and whole gene repertoire comparison of the EHECs and other fully sequenced E. coli/Shigella strains. (A) The neighbor-joining tree constructed by using the concatenated nucleotide sequences of 345 orthologous CDS groups from the 25 sequenced strains. These CDS groups were selected as nonrecombinogenic CDS groups by using the PHI-test (cut off value: P ≥ 0.05), from 926 orthologous CDS groups, in which all members of each group were conserved and of same length in all of the 25 strains. Locus tags of the 345 and 926 CDSs in K-12 MG1655 are listed in the legend of Fig. S1. The reliability of the internal branches was assessed by bootstrapping with 250 pseudoreplicates. The E. coli phylogroup (A, B1, B2, D, or E) of each strain is indicated in brackets. Pathotypes of the strains are indicated by different colors (see Table S1 for the details of the strains). (Scale bar: number of substitutions per site.) (B) The hierarchical clustering tree that was constructed based on a gene repertoire comparison of the 25 strains. The entire gene repertoire of the 25 strains is represented by 12,940 CDS groups that were defined based on the results of an all-to-all BLASTP analysis of CDSs from the 25 strains.
Fig. 4.
Fig. 4.
The genetic organization of the LEEs and SpLE3-like IEs identified in the 4 EHEC genomes is shown. Homologous regions are indicated by purple shading.
Fig. 5.
Fig. 5.
The gene organization of the effector exchangeable loci (of lambdoid PPs identified in the 4 EHEC strains is shown. Effector exchangeable loci are located just downstream of the tail fiber genes and contain various T3SS effector genes. Pseudogenes are indicated by asterisks.

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