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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Public Library of Science (PLoS)
2009
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oai:doaj.org-article:fd07a3c5bce543f5b43e97b5003a63df2021-12-02T19:59:47ZGenomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens.1553-73661553-737410.1371/journal.ppat.1000346https://doaj.org/article/fd07a3c5bce543f5b43e97b5003a63df2009-03-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/19325880/pdf/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374The 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.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 WallerPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 5, Iss 3, p e1000346 (2009) |
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Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 |
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Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 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. |
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. |
format |
article |
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 |
title |
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_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_sort |
genomic evidence for the evolution of streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2009 |
url |
https://doaj.org/article/fd07a3c5bce543f5b43e97b5003a63df |
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