Limits...
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.

Show MeSH

Related in: MedlinePlus

Schematic circular diagrams of the Se4047 (A) and SzH70 genomes (B).Key for the circular diagrams (outside to inside): scale (in Mb); annotated CDSs colored according to predicted function represented on a pair of concentric circles, representing both coding strands; orthologue matches shared with the Streptococcal species, Se4047 or SzH70, SzMGCS10565, S. uberis 0140J, S. pyogenes Manfredo, S. mutans UA159, S. gordonii Challis CH1, S. sanguinis SK36, S. pneumoniae TIGR4, S. agalactiae NEM316, S. suis P1/7, S. thermophilus CNRZ1066, blue; orthologue matches shared with Lactococcus lactis subspecies lactis, green; G+C% content plot; G+C deviation plot (>0%, olive, <0%, purple). Color coding for CDS functions: dark blue, pathogenicity/adaptation; black, energy metabolism; red, information transfer; dark green, surface-associated; cyan, degradation of large molecules; magenta, degradation of small molecules; yellow, central/intermediary metabolism; pale green, unknown; pale blue, regulators; orange, conserved hypothetical; brown, pseudogenes; pink, phage and IS elements; grey, miscellaneous. The positions of the four prophage and two ICESe present in the Se4047 genome, and two ICESz in the SzH70 genome, are indicated.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2654543&req=5

ppat-1000346-g001: Schematic circular diagrams of the Se4047 (A) and SzH70 genomes (B).Key for the circular diagrams (outside to inside): scale (in Mb); annotated CDSs colored according to predicted function represented on a pair of concentric circles, representing both coding strands; orthologue matches shared with the Streptococcal species, Se4047 or SzH70, SzMGCS10565, S. uberis 0140J, S. pyogenes Manfredo, S. mutans UA159, S. gordonii Challis CH1, S. sanguinis SK36, S. pneumoniae TIGR4, S. agalactiae NEM316, S. suis P1/7, S. thermophilus CNRZ1066, blue; orthologue matches shared with Lactococcus lactis subspecies lactis, green; G+C% content plot; G+C deviation plot (>0%, olive, <0%, purple). Color coding for CDS functions: dark blue, pathogenicity/adaptation; black, energy metabolism; red, information transfer; dark green, surface-associated; cyan, degradation of large molecules; magenta, degradation of small molecules; yellow, central/intermediary metabolism; pale green, unknown; pale blue, regulators; orange, conserved hypothetical; brown, pseudogenes; pink, phage and IS elements; grey, miscellaneous. The positions of the four prophage and two ICESe present in the Se4047 genome, and two ICESz in the SzH70 genome, are indicated.

Mentions: Multilocus sequence typing (MLST) has provided evidence of the close genetic relationship of S. equi and S. zooepidemicus [2]. The genomes of Se4047 (ST-179) and SzH70 (ST-1) support the overall relatedness, but also reveal evidence of genome plasticity that has generated notable diversity. The two genomes are similar in size: the Se4047 genome consists of a circular chromosome of 2,253,793 bp (Figure 1A) encoding 2,137 predicted coding sequences (CDSs), and the SzH70 genome contains a chromosome of 2,149,866 bp (Figure 1B), encoding 1,960 predicted CDSs. Much of the Se4047 genome is orthologous to the SzH70 genome: 1671 Se4047 CDSs have SzH70 orthologs. Of the remaining 466 non-orthologous Se4047 CDSs, 422 are found on mobile genetic elements (MGEs; for details of the regions of variation in the Se4047 and SzH70 genomes see Table S1).


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)

Schematic circular diagrams of the Se4047 (A) and SzH70 genomes (B).Key for the circular diagrams (outside to inside): scale (in Mb); annotated CDSs colored according to predicted function represented on a pair of concentric circles, representing both coding strands; orthologue matches shared with the Streptococcal species, Se4047 or SzH70, SzMGCS10565, S. uberis 0140J, S. pyogenes Manfredo, S. mutans UA159, S. gordonii Challis CH1, S. sanguinis SK36, S. pneumoniae TIGR4, S. agalactiae NEM316, S. suis P1/7, S. thermophilus CNRZ1066, blue; orthologue matches shared with Lactococcus lactis subspecies lactis, green; G+C% content plot; G+C deviation plot (>0%, olive, <0%, purple). Color coding for CDS functions: dark blue, pathogenicity/adaptation; black, energy metabolism; red, information transfer; dark green, surface-associated; cyan, degradation of large molecules; magenta, degradation of small molecules; yellow, central/intermediary metabolism; pale green, unknown; pale blue, regulators; orange, conserved hypothetical; brown, pseudogenes; pink, phage and IS elements; grey, miscellaneous. The positions of the four prophage and two ICESe present in the Se4047 genome, and two ICESz in the SzH70 genome, are indicated.
© Copyright Policy
Related In: Results  -  Collection

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

ppat-1000346-g001: Schematic circular diagrams of the Se4047 (A) and SzH70 genomes (B).Key for the circular diagrams (outside to inside): scale (in Mb); annotated CDSs colored according to predicted function represented on a pair of concentric circles, representing both coding strands; orthologue matches shared with the Streptococcal species, Se4047 or SzH70, SzMGCS10565, S. uberis 0140J, S. pyogenes Manfredo, S. mutans UA159, S. gordonii Challis CH1, S. sanguinis SK36, S. pneumoniae TIGR4, S. agalactiae NEM316, S. suis P1/7, S. thermophilus CNRZ1066, blue; orthologue matches shared with Lactococcus lactis subspecies lactis, green; G+C% content plot; G+C deviation plot (>0%, olive, <0%, purple). Color coding for CDS functions: dark blue, pathogenicity/adaptation; black, energy metabolism; red, information transfer; dark green, surface-associated; cyan, degradation of large molecules; magenta, degradation of small molecules; yellow, central/intermediary metabolism; pale green, unknown; pale blue, regulators; orange, conserved hypothetical; brown, pseudogenes; pink, phage and IS elements; grey, miscellaneous. The positions of the four prophage and two ICESe present in the Se4047 genome, and two ICESz in the SzH70 genome, are indicated.
Mentions: Multilocus sequence typing (MLST) has provided evidence of the close genetic relationship of S. equi and S. zooepidemicus [2]. The genomes of Se4047 (ST-179) and SzH70 (ST-1) support the overall relatedness, but also reveal evidence of genome plasticity that has generated notable diversity. The two genomes are similar in size: the Se4047 genome consists of a circular chromosome of 2,253,793 bp (Figure 1A) encoding 2,137 predicted coding sequences (CDSs), and the SzH70 genome contains a chromosome of 2,149,866 bp (Figure 1B), encoding 1,960 predicted CDSs. Much of the Se4047 genome is orthologous to the SzH70 genome: 1671 Se4047 CDSs have SzH70 orthologs. Of the remaining 466 non-orthologous Se4047 CDSs, 422 are found on mobile genetic elements (MGEs; for details of the regions of variation in the Se4047 and SzH70 genomes see Table S1).

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