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

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...

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Main Authors: Matthew T G Holden, Zoe Heather, Romain Paillot, Karen F Steward, Katy Webb, Fern Ainslie, Thibaud Jourdan, Nathalie C Bason, Nancy E Holroyd, Karen Mungall, Michael A Quail, Mandy Sanders, Mark Simmonds, David Willey, Karen Brooks, David M Aanensen, Brian G Spratt, Keith A Jolley, Martin C J Maiden, Michael Kehoe, Neil Chanter, Stephen D Bentley, Carl Robinson, Duncan J Maskell, Julian Parkhill, Andrew S Waller
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2009-03-01
Series:PLoS Pathogens
Online Access:https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1000346&type=printable
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author Matthew T G Holden
Zoe Heather
Romain Paillot
Karen F Steward
Katy Webb
Fern Ainslie
Thibaud Jourdan
Nathalie C Bason
Nancy E Holroyd
Karen Mungall
Michael A Quail
Mandy Sanders
Mark Simmonds
David Willey
Karen Brooks
David M Aanensen
Brian G Spratt
Keith A Jolley
Martin C J Maiden
Michael Kehoe
Neil Chanter
Stephen D Bentley
Carl Robinson
Duncan J Maskell
Julian Parkhill
Andrew S Waller
author_facet Matthew T G Holden
Zoe Heather
Romain Paillot
Karen F Steward
Katy Webb
Fern Ainslie
Thibaud Jourdan
Nathalie C Bason
Nancy E Holroyd
Karen Mungall
Michael A Quail
Mandy Sanders
Mark Simmonds
David Willey
Karen Brooks
David M Aanensen
Brian G Spratt
Keith A Jolley
Martin C J Maiden
Michael Kehoe
Neil Chanter
Stephen D Bentley
Carl Robinson
Duncan J Maskell
Julian Parkhill
Andrew S Waller
author_sort Matthew T G Holden
collection DOAJ
description 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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spelling doaj-art-fd07a3c5bce543f5b43e97b5003a63df2025-08-20T02:00:50ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742009-03-0153e100034610.1371/journal.ppat.1000346Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens.Matthew T G HoldenZoe HeatherRomain PaillotKaren F StewardKaty WebbFern AinslieThibaud JourdanNathalie C BasonNancy E HolroydKaren MungallMichael A QuailMandy SandersMark SimmondsDavid WilleyKaren BrooksDavid M AanensenBrian G SprattKeith A JolleyMartin C J MaidenMichael KehoeNeil ChanterStephen D BentleyCarl RobinsonDuncan J MaskellJulian ParkhillAndrew S WallerThe 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.https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1000346&type=printable
spellingShingle Matthew T G Holden
Zoe Heather
Romain Paillot
Karen F Steward
Katy Webb
Fern Ainslie
Thibaud Jourdan
Nathalie C Bason
Nancy E Holroyd
Karen Mungall
Michael A Quail
Mandy Sanders
Mark Simmonds
David Willey
Karen Brooks
David M Aanensen
Brian G Spratt
Keith A Jolley
Martin C J Maiden
Michael Kehoe
Neil Chanter
Stephen D Bentley
Carl Robinson
Duncan J Maskell
Julian Parkhill
Andrew S Waller
Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens.
PLoS Pathogens
title Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens.
title_full Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens.
title_fullStr Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens.
title_full_unstemmed Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens.
title_short Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens.
title_sort genomic evidence for the evolution of streptococcus equi host restriction increased virulence and genetic exchange with human pathogens
url https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1000346&type=printable
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