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Evolution of enterohemorrhagic escherichia coli O26 based on single-nucleotide polymorphisms.

Bletz S, Bielaszewska M, Leopold SR, Köck R, Witten A, Schuldes J, Zhang W, Karch H, Mellmann A - Genome Biol Evol (2013)

Bottom Line: Within approximately 1 Mb of core genes, WGS resulted in 476 high-quality bi-allelic SNP localizations.SNP-CC2 was significantly associated with the development of HUS.WGS and subsequent SNP typing enabled us to gain new insights into the evolution of EHEC O26 suggesting a common theme in this EHEC group with analogies to EHEC O157.

View Article: PubMed Central - PubMed

Affiliation: Institute of Hygiene, University of Münster, Germany.

ABSTRACT
Enterohemorrhagic Escherichia coli (EHEC) O26:H11/H⁻ is the predominant non-O157 EHEC serotype among patients with diarrhea, bloody diarrhea, and hemolytic uremic syndrome (HUS) worldwide. To elucidate their phylogeny and association between their phylogenetic background and clinical outcome of the infection, we investigated 120 EHEC O26:H11/H⁻ strains isolated between 1965 and 2012 from asymptomatic carriers and patients with diarrhea or HUS. Whole-genome shotgun sequencing (WGS) was applied to ten representative EHEC O26 isolates to determine single nucleotide polymorphism (SNP) localizations within a predefined set of core genes. A multiplex SNP assay, comprising a randomly distributed subset of 48 SNPs, was established to detect SNPs in 110 additional EHEC O26 strains. Within approximately 1 Mb of core genes, WGS resulted in 476 high-quality bi-allelic SNP localizations. Forty-eight of these were subsequently investigated in 110 EHEC O26 and four different SNP clonal complexes (SNP-CC) were identified. SNP-CC2 was significantly associated with the development of HUS. Within the subsequently established evolutionary model of EHEC O26, we dated the emergence of human EHEC O26 to approximately 19,700 years ago and demonstrated a recent evolution within humans into the 4 SNP-CCs over the past 1,650 years. WGS and subsequent SNP typing enabled us to gain new insights into the evolution of EHEC O26 suggesting a common theme in this EHEC group with analogies to EHEC O157. In addition, the SNP-CC analysis may help to assess a risk in infected individuals for the progression to HUS and to implement more specific infection control measures.

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Evolutionary model and calculated age distances for EHEC O26 pathogens based on the neighbor-joining tree (fig. 3) and inserted in the SNP clonal clusters (SNP-CC1 to SNP-CC4). Blue boxes are the EHEC O26 isolates with shotgun genome sequencing data. In gray, hypothetical founders of O26 isolates are shown (A01 to A10). The ancestry is calculated based on the phylogeny displayed in figure 3. White boxes show the two EHEC O26:H11 and EHEC O111:H− reference strains (strains 11368 and 11128, respectively) that are fully sequenced; EHEC O111:H− is assumed to be the closest relative of serogroup O26 (Whittam et al. 1988). Blue lines connect the isolates and the hypothetical ancestors and red numbers show the synonymous/nonsynonymous SNPs between these genotypes. The gray line connects the O111:H− reference strain and the first O26 ancestor A10 as the common O26/O111 ancestor is not known. Distances are not drawn to scale.
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evt136-F4: Evolutionary model and calculated age distances for EHEC O26 pathogens based on the neighbor-joining tree (fig. 3) and inserted in the SNP clonal clusters (SNP-CC1 to SNP-CC4). Blue boxes are the EHEC O26 isolates with shotgun genome sequencing data. In gray, hypothetical founders of O26 isolates are shown (A01 to A10). The ancestry is calculated based on the phylogeny displayed in figure 3. White boxes show the two EHEC O26:H11 and EHEC O111:H− reference strains (strains 11368 and 11128, respectively) that are fully sequenced; EHEC O111:H− is assumed to be the closest relative of serogroup O26 (Whittam et al. 1988). Blue lines connect the isolates and the hypothetical ancestors and red numbers show the synonymous/nonsynonymous SNPs between these genotypes. The gray line connects the O111:H− reference strain and the first O26 ancestor A10 as the common O26/O111 ancestor is not known. Distances are not drawn to scale.

Mentions: The phylogenetic topology of the ten representative EHEC O26 isolates (supplementary table S1, Supplementary Material online), the O26:H11 reference strain 11368 and, as an outgroup, the next closely related EHEC serotype O111:H− strain 11128 (NC_013364.1) (Ogura et al. 2009; Ju et al. 2012) are shown in a neighbor-joining tree (fig. 3). The branching within this tree was concordant to the separation based on the SNP assay (fig. 2) underlining the unbiased representativeness of the selected 48 SNP localizations. We propose an evolutionary model of EHEC O26 with a subdivision into four SNP-CCs. Using the Ks values (number of synonymous substitutions per synonymous site) of strains 11128 (EHEC O111) and A10, along with hypothetical intermediate isolates A01 to A10 and a common ancestor of E. coli O26 and O111 as previously proposed (Whittam et al. 1988), we postulate that E. coli O26 and O111 separated 19,700 years ago (fig. 4). Since then, EHEC O26 likely developed sequentially from SNP-CC1 to SNP-CC4. The evolution of these clonal clusters occurred within 1,650 years of this bifurcation (fig. 4). During this evolution, there was a parallel evolution of the core genome and stx as the most important virulence marker as both were almost exclusively associated in a fixed combination within the different SNP-CCs (fig. 4).Fig. 3.—


Evolution of enterohemorrhagic escherichia coli O26 based on single-nucleotide polymorphisms.

Bletz S, Bielaszewska M, Leopold SR, Köck R, Witten A, Schuldes J, Zhang W, Karch H, Mellmann A - Genome Biol Evol (2013)

Evolutionary model and calculated age distances for EHEC O26 pathogens based on the neighbor-joining tree (fig. 3) and inserted in the SNP clonal clusters (SNP-CC1 to SNP-CC4). Blue boxes are the EHEC O26 isolates with shotgun genome sequencing data. In gray, hypothetical founders of O26 isolates are shown (A01 to A10). The ancestry is calculated based on the phylogeny displayed in figure 3. White boxes show the two EHEC O26:H11 and EHEC O111:H− reference strains (strains 11368 and 11128, respectively) that are fully sequenced; EHEC O111:H− is assumed to be the closest relative of serogroup O26 (Whittam et al. 1988). Blue lines connect the isolates and the hypothetical ancestors and red numbers show the synonymous/nonsynonymous SNPs between these genotypes. The gray line connects the O111:H− reference strain and the first O26 ancestor A10 as the common O26/O111 ancestor is not known. Distances are not drawn to scale.
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Related In: Results  -  Collection

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evt136-F4: Evolutionary model and calculated age distances for EHEC O26 pathogens based on the neighbor-joining tree (fig. 3) and inserted in the SNP clonal clusters (SNP-CC1 to SNP-CC4). Blue boxes are the EHEC O26 isolates with shotgun genome sequencing data. In gray, hypothetical founders of O26 isolates are shown (A01 to A10). The ancestry is calculated based on the phylogeny displayed in figure 3. White boxes show the two EHEC O26:H11 and EHEC O111:H− reference strains (strains 11368 and 11128, respectively) that are fully sequenced; EHEC O111:H− is assumed to be the closest relative of serogroup O26 (Whittam et al. 1988). Blue lines connect the isolates and the hypothetical ancestors and red numbers show the synonymous/nonsynonymous SNPs between these genotypes. The gray line connects the O111:H− reference strain and the first O26 ancestor A10 as the common O26/O111 ancestor is not known. Distances are not drawn to scale.
Mentions: The phylogenetic topology of the ten representative EHEC O26 isolates (supplementary table S1, Supplementary Material online), the O26:H11 reference strain 11368 and, as an outgroup, the next closely related EHEC serotype O111:H− strain 11128 (NC_013364.1) (Ogura et al. 2009; Ju et al. 2012) are shown in a neighbor-joining tree (fig. 3). The branching within this tree was concordant to the separation based on the SNP assay (fig. 2) underlining the unbiased representativeness of the selected 48 SNP localizations. We propose an evolutionary model of EHEC O26 with a subdivision into four SNP-CCs. Using the Ks values (number of synonymous substitutions per synonymous site) of strains 11128 (EHEC O111) and A10, along with hypothetical intermediate isolates A01 to A10 and a common ancestor of E. coli O26 and O111 as previously proposed (Whittam et al. 1988), we postulate that E. coli O26 and O111 separated 19,700 years ago (fig. 4). Since then, EHEC O26 likely developed sequentially from SNP-CC1 to SNP-CC4. The evolution of these clonal clusters occurred within 1,650 years of this bifurcation (fig. 4). During this evolution, there was a parallel evolution of the core genome and stx as the most important virulence marker as both were almost exclusively associated in a fixed combination within the different SNP-CCs (fig. 4).Fig. 3.—

Bottom Line: Within approximately 1 Mb of core genes, WGS resulted in 476 high-quality bi-allelic SNP localizations.SNP-CC2 was significantly associated with the development of HUS.WGS and subsequent SNP typing enabled us to gain new insights into the evolution of EHEC O26 suggesting a common theme in this EHEC group with analogies to EHEC O157.

View Article: PubMed Central - PubMed

Affiliation: Institute of Hygiene, University of Münster, Germany.

ABSTRACT
Enterohemorrhagic Escherichia coli (EHEC) O26:H11/H⁻ is the predominant non-O157 EHEC serotype among patients with diarrhea, bloody diarrhea, and hemolytic uremic syndrome (HUS) worldwide. To elucidate their phylogeny and association between their phylogenetic background and clinical outcome of the infection, we investigated 120 EHEC O26:H11/H⁻ strains isolated between 1965 and 2012 from asymptomatic carriers and patients with diarrhea or HUS. Whole-genome shotgun sequencing (WGS) was applied to ten representative EHEC O26 isolates to determine single nucleotide polymorphism (SNP) localizations within a predefined set of core genes. A multiplex SNP assay, comprising a randomly distributed subset of 48 SNPs, was established to detect SNPs in 110 additional EHEC O26 strains. Within approximately 1 Mb of core genes, WGS resulted in 476 high-quality bi-allelic SNP localizations. Forty-eight of these were subsequently investigated in 110 EHEC O26 and four different SNP clonal complexes (SNP-CC) were identified. SNP-CC2 was significantly associated with the development of HUS. Within the subsequently established evolutionary model of EHEC O26, we dated the emergence of human EHEC O26 to approximately 19,700 years ago and demonstrated a recent evolution within humans into the 4 SNP-CCs over the past 1,650 years. WGS and subsequent SNP typing enabled us to gain new insights into the evolution of EHEC O26 suggesting a common theme in this EHEC group with analogies to EHEC O157. In addition, the SNP-CC analysis may help to assess a risk in infected individuals for the progression to HUS and to implement more specific infection control measures.

Show MeSH
Related in: MedlinePlus