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Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens.

Holden MT, Heather Z, Paillot R, Steward KF, Webb K, Ainslie F, Jourdan T, Bason NC, Holroyd NE, Mungall K, Quail MA, Sanders M, Simmonds M, Willey D, Brooks K, Aanensen DM, Spratt BG, Jolley KA, Maiden MC, Kehoe M, Chanter N, Bentley SD, Robinson C, Maskell DJ, Parkhill J, Waller AS - PLoS Pathog. (2009)

Bottom Line: We sequenced and compared the genomes of S. equi 4047 and S. zooepidemicus H70 and screened S. equi and S. zooepidemicus strains from around the world to uncover evidence of the genetic events that have shaped the evolution of the S. equi genome and led to its emergence as a host-restricted pathogen.We also highlight that S. equi, S. zooepidemicus, and S. pyogenes share a common phage pool that enhances cross-species pathogen evolution.We conclude that the complex interplay of functional loss, pathogenic specialization, and genetic exchange between S. equi, S. zooepidemicus, and S. pyogenes continues to influence the evolution of these important streptococci.

View Article: PubMed Central - PubMed

Affiliation: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom.

ABSTRACT
The continued evolution of bacterial pathogens has major implications for both human and animal disease, but the exchange of genetic material between host-restricted pathogens is rarely considered. Streptococcus equi subspecies equi (S. equi) is a host-restricted pathogen of horses that has evolved from the zoonotic pathogen Streptococcus equi subspecies zooepidemicus (S. zooepidemicus). These pathogens share approximately 80% genome sequence identity with the important human pathogen Streptococcus pyogenes. We sequenced and compared the genomes of S. equi 4047 and S. zooepidemicus H70 and screened S. equi and S. zooepidemicus strains from around the world to uncover evidence of the genetic events that have shaped the evolution of the S. equi genome and led to its emergence as a host-restricted pathogen. Our analysis provides evidence of functional loss due to mutation and deletion, coupled with pathogenic specialization through the acquisition of bacteriophage encoding a phospholipase A(2) toxin, and four superantigens, and an integrative conjugative element carrying a novel iron acquisition system with similarity to the high pathogenicity island of Yersinia pestis. We also highlight that S. equi, S. zooepidemicus, and S. pyogenes share a common phage pool that enhances cross-species pathogen evolution. We conclude that the complex interplay of functional loss, pathogenic specialization, and genetic exchange between S. equi, S. zooepidemicus, and S. pyogenes continues to influence the evolution of these important streptococci.

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Pairwise comparison of the chromosomes of Se4047 and SzH70 using ACT.The sequences have been aligned from the predicted replication origins (oriC; right). The colored bars separating each genome (red and blue) represent similarity matches identified by reciprocal TBLASTX analysis [71], with a score cutoff of 100. Red lines link matches in the same orientation; blue lines link matches in the reverse orientation. The prophage (pink) and ICE (purple) are highlighted as colored boxes.
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ppat-1000346-g002: Pairwise comparison of the chromosomes of Se4047 and SzH70 using ACT.The sequences have been aligned from the predicted replication origins (oriC; right). The colored bars separating each genome (red and blue) represent similarity matches identified by reciprocal TBLASTX analysis [71], with a score cutoff of 100. Red lines link matches in the same orientation; blue lines link matches in the reverse orientation. The prophage (pink) and ICE (purple) are highlighted as colored boxes.

Mentions: The chromosomes of Se4047 and SzH70 are generally collinear except for two inversions around the origin of replication (Figure 2). The smaller central inversion is due to recombination events in Se4047 between identical ISSeq3 elements on opposite replichores. The larger rearrangement is due to an inter-replichore inversion in SzH70 of unknown origin (Figure 2). Both the Se4047 and SzH70 genomes contain two copies of hasC which encode UDP-glucose pyrophosphorylases [14]. In SzH70 one copy of hasC (SZO17510) has been translocated to the opposite replichore by the previously mentioned large reciprocal inversion. There is also a small intra-replichore inversion (∼14 kb) in Se4047 between the two copies of hasC (SEQ0271 and SEQ0289). The hasC-mediated inversion in Se4047 rearranges the genes associated with capsule production [14] and may explain why S. equi produces such high levels of hyaluronate capsule.


Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens.

Holden MT, Heather Z, Paillot R, Steward KF, Webb K, Ainslie F, Jourdan T, Bason NC, Holroyd NE, Mungall K, Quail MA, Sanders M, Simmonds M, Willey D, Brooks K, Aanensen DM, Spratt BG, Jolley KA, Maiden MC, Kehoe M, Chanter N, Bentley SD, Robinson C, Maskell DJ, Parkhill J, Waller AS - PLoS Pathog. (2009)

Pairwise comparison of the chromosomes of Se4047 and SzH70 using ACT.The sequences have been aligned from the predicted replication origins (oriC; right). The colored bars separating each genome (red and blue) represent similarity matches identified by reciprocal TBLASTX analysis [71], with a score cutoff of 100. Red lines link matches in the same orientation; blue lines link matches in the reverse orientation. The prophage (pink) and ICE (purple) are highlighted as colored boxes.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2654543&req=5

ppat-1000346-g002: Pairwise comparison of the chromosomes of Se4047 and SzH70 using ACT.The sequences have been aligned from the predicted replication origins (oriC; right). The colored bars separating each genome (red and blue) represent similarity matches identified by reciprocal TBLASTX analysis [71], with a score cutoff of 100. Red lines link matches in the same orientation; blue lines link matches in the reverse orientation. The prophage (pink) and ICE (purple) are highlighted as colored boxes.
Mentions: The chromosomes of Se4047 and SzH70 are generally collinear except for two inversions around the origin of replication (Figure 2). The smaller central inversion is due to recombination events in Se4047 between identical ISSeq3 elements on opposite replichores. The larger rearrangement is due to an inter-replichore inversion in SzH70 of unknown origin (Figure 2). Both the Se4047 and SzH70 genomes contain two copies of hasC which encode UDP-glucose pyrophosphorylases [14]. In SzH70 one copy of hasC (SZO17510) has been translocated to the opposite replichore by the previously mentioned large reciprocal inversion. There is also a small intra-replichore inversion (∼14 kb) in Se4047 between the two copies of hasC (SEQ0271 and SEQ0289). The hasC-mediated inversion in Se4047 rearranges the genes associated with capsule production [14] and may explain why S. equi produces such high levels of hyaluronate capsule.

Bottom Line: We sequenced and compared the genomes of S. equi 4047 and S. zooepidemicus H70 and screened S. equi and S. zooepidemicus strains from around the world to uncover evidence of the genetic events that have shaped the evolution of the S. equi genome and led to its emergence as a host-restricted pathogen.We also highlight that S. equi, S. zooepidemicus, and S. pyogenes share a common phage pool that enhances cross-species pathogen evolution.We conclude that the complex interplay of functional loss, pathogenic specialization, and genetic exchange between S. equi, S. zooepidemicus, and S. pyogenes continues to influence the evolution of these important streptococci.

View Article: PubMed Central - PubMed

Affiliation: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom.

ABSTRACT
The continued evolution of bacterial pathogens has major implications for both human and animal disease, but the exchange of genetic material between host-restricted pathogens is rarely considered. Streptococcus equi subspecies equi (S. equi) is a host-restricted pathogen of horses that has evolved from the zoonotic pathogen Streptococcus equi subspecies zooepidemicus (S. zooepidemicus). These pathogens share approximately 80% genome sequence identity with the important human pathogen Streptococcus pyogenes. We sequenced and compared the genomes of S. equi 4047 and S. zooepidemicus H70 and screened S. equi and S. zooepidemicus strains from around the world to uncover evidence of the genetic events that have shaped the evolution of the S. equi genome and led to its emergence as a host-restricted pathogen. Our analysis provides evidence of functional loss due to mutation and deletion, coupled with pathogenic specialization through the acquisition of bacteriophage encoding a phospholipase A(2) toxin, and four superantigens, and an integrative conjugative element carrying a novel iron acquisition system with similarity to the high pathogenicity island of Yersinia pestis. We also highlight that S. equi, S. zooepidemicus, and S. pyogenes share a common phage pool that enhances cross-species pathogen evolution. We conclude that the complex interplay of functional loss, pathogenic specialization, and genetic exchange between S. equi, S. zooepidemicus, and S. pyogenes continues to influence the evolution of these important streptococci.

Show MeSH
Related in: MedlinePlus