Identification of Virulence-Associated Properties by Comparative Genome Analysis of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>, <named-content content-type="genus-species">S. pseudopneumoniae</named-content>, <named-content content-type="genus-species">S. mitis</named-content>, Three <named-content content-type="genus-species">S. oralis</named-content> Subspecies, and <italic toggle="yes">S. infantis</italic>

ABSTRACT From a common ancestor, Streptococcus pneumoniae and Streptococcus mitis evolved in parallel into one of the most important pathogens and a mutualistic colonizer of humans, respectively. This evolutionary scenario provides a unique basis for studies of both infection-associated properties a...

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Autores principales:	Mogens Kilian, Hervé Tettelin
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Streptococcus mitis Streptococcus oralis Streptococcus pneumoniae bacteremia commensal evolution Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7af388da477d402f8d9ba062aa7524df
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spelling	oai:doaj.org-article:7af388da477d402f8d9ba062aa7524df2021-11-15T15:59:41ZIdentification of Virulence-Associated Properties by Comparative Genome Analysis of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>, <named-content content-type="genus-species">S. pseudopneumoniae</named-content>, <named-content content-type="genus-species">S. mitis</named-content>, Three <named-content content-type="genus-species">S. oralis</named-content> Subspecies, and <italic toggle="yes">S. infantis</italic>10.1128/mBio.01985-192150-7511https://doaj.org/article/7af388da477d402f8d9ba062aa7524df2019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01985-19https://doaj.org/toc/2150-7511ABSTRACT From a common ancestor, Streptococcus pneumoniae and Streptococcus mitis evolved in parallel into one of the most important pathogens and a mutualistic colonizer of humans, respectively. This evolutionary scenario provides a unique basis for studies of both infection-associated properties and properties important for harmonious coexistence with the host. We performed detailed comparisons of 60 genomes of S. pneumoniae, S. mitis, Streptococcus pseudopneumoniae, the three Streptococcus oralis subspecies oralis, tigurinus, and dentisani, and Streptococcus infantis. Nonfunctional remnants of ancestral genes in both S. pneumoniae and in S. mitis support the evolutionary model and the concept that evolutionary changes on both sides were required to reach their present relationship to the host. Confirmed by screening of >7,500 genomes, we identified 224 genes associated with virulence. The striking difference to commensal streptococci was the diversity of regulatory mechanisms, including regulation of capsule production, a significantly larger arsenal of enzymes involved in carbohydrate hydrolysis, and proteins known to interfere with innate immune factors. The exclusive presence of the virulence factors in S. pneumoniae enhances their potential as vaccine components, as a direct impact on beneficial members of the commensal microbiota can be excluded. In addition to loss of these virulence-associated genes, adaptation of S. mitis to a mutualistic relationship with the host apparently required preservation or acquisition of 25 genes lost or absent from S. pneumoniae. Successful adaptation of S. mitis and other commensal streptococci to a harmonious relationship with the host relied on genetic stability and properties facilitating life in biofilms. IMPORTANCE Streptococcus pneumoniae is one of the most important human pathogens but is closely related to Streptococcus mitis, with which humans live in harmony. The fact that the two species evolved from a common ancestor provides a unique basis for studies of both infection-associated properties and properties important for harmonious coexistence with the host. By detailed comparisons of genomes of the two species and other related streptococci, we identified 224 genes associated with virulence and 25 genes unique to the mutualistic species. The exclusive presence of the virulence factors in S. pneumoniae enhances their potential as vaccine components, as a direct impact on beneficial members of the commensal microbiota can be excluded. Successful adaptation of S. mitis and other commensal streptococci to a harmonious relationship with the host relied on genetic stability and properties facilitating life in biofilms.Mogens KilianHervé TettelinAmerican Society for MicrobiologyarticleStreptococcus mitisStreptococcus oralisStreptococcus pneumoniaebacteremiacommensalevolutionMicrobiologyQR1-502ENmBio, Vol 10, Iss 5 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Streptococcus mitis Streptococcus oralis Streptococcus pneumoniae bacteremia commensal evolution Microbiology QR1-502
spellingShingle	Streptococcus mitis Streptococcus oralis Streptococcus pneumoniae bacteremia commensal evolution Microbiology QR1-502 Mogens Kilian Hervé Tettelin Identification of Virulence-Associated Properties by Comparative Genome Analysis of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>, <named-content content-type="genus-species">S. pseudopneumoniae</named-content>, <named-content content-type="genus-species">S. mitis</named-content>, Three <named-content content-type="genus-species">S. oralis</named-content> Subspecies, and <italic toggle="yes">S. infantis</italic>
description	ABSTRACT From a common ancestor, Streptococcus pneumoniae and Streptococcus mitis evolved in parallel into one of the most important pathogens and a mutualistic colonizer of humans, respectively. This evolutionary scenario provides a unique basis for studies of both infection-associated properties and properties important for harmonious coexistence with the host. We performed detailed comparisons of 60 genomes of S. pneumoniae, S. mitis, Streptococcus pseudopneumoniae, the three Streptococcus oralis subspecies oralis, tigurinus, and dentisani, and Streptococcus infantis. Nonfunctional remnants of ancestral genes in both S. pneumoniae and in S. mitis support the evolutionary model and the concept that evolutionary changes on both sides were required to reach their present relationship to the host. Confirmed by screening of >7,500 genomes, we identified 224 genes associated with virulence. The striking difference to commensal streptococci was the diversity of regulatory mechanisms, including regulation of capsule production, a significantly larger arsenal of enzymes involved in carbohydrate hydrolysis, and proteins known to interfere with innate immune factors. The exclusive presence of the virulence factors in S. pneumoniae enhances their potential as vaccine components, as a direct impact on beneficial members of the commensal microbiota can be excluded. In addition to loss of these virulence-associated genes, adaptation of S. mitis to a mutualistic relationship with the host apparently required preservation or acquisition of 25 genes lost or absent from S. pneumoniae. Successful adaptation of S. mitis and other commensal streptococci to a harmonious relationship with the host relied on genetic stability and properties facilitating life in biofilms. IMPORTANCE Streptococcus pneumoniae is one of the most important human pathogens but is closely related to Streptococcus mitis, with which humans live in harmony. The fact that the two species evolved from a common ancestor provides a unique basis for studies of both infection-associated properties and properties important for harmonious coexistence with the host. By detailed comparisons of genomes of the two species and other related streptococci, we identified 224 genes associated with virulence and 25 genes unique to the mutualistic species. The exclusive presence of the virulence factors in S. pneumoniae enhances their potential as vaccine components, as a direct impact on beneficial members of the commensal microbiota can be excluded. Successful adaptation of S. mitis and other commensal streptococci to a harmonious relationship with the host relied on genetic stability and properties facilitating life in biofilms.
format	article
author	Mogens Kilian Hervé Tettelin
author_facet	Mogens Kilian Hervé Tettelin
author_sort	Mogens Kilian
title	Identification of Virulence-Associated Properties by Comparative Genome Analysis of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>, <named-content content-type="genus-species">S. pseudopneumoniae</named-content>, <named-content content-type="genus-species">S. mitis</named-content>, Three <named-content content-type="genus-species">S. oralis</named-content> Subspecies, and <italic toggle="yes">S. infantis</italic>
title_short	Identification of Virulence-Associated Properties by Comparative Genome Analysis of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>, <named-content content-type="genus-species">S. pseudopneumoniae</named-content>, <named-content content-type="genus-species">S. mitis</named-content>, Three <named-content content-type="genus-species">S. oralis</named-content> Subspecies, and <italic toggle="yes">S. infantis</italic>
title_full	Identification of Virulence-Associated Properties by Comparative Genome Analysis of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>, <named-content content-type="genus-species">S. pseudopneumoniae</named-content>, <named-content content-type="genus-species">S. mitis</named-content>, Three <named-content content-type="genus-species">S. oralis</named-content> Subspecies, and <italic toggle="yes">S. infantis</italic>
title_fullStr	Identification of Virulence-Associated Properties by Comparative Genome Analysis of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>, <named-content content-type="genus-species">S. pseudopneumoniae</named-content>, <named-content content-type="genus-species">S. mitis</named-content>, Three <named-content content-type="genus-species">S. oralis</named-content> Subspecies, and <italic toggle="yes">S. infantis</italic>
title_full_unstemmed	Identification of Virulence-Associated Properties by Comparative Genome Analysis of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content>, <named-content content-type="genus-species">S. pseudopneumoniae</named-content>, <named-content content-type="genus-species">S. mitis</named-content>, Three <named-content content-type="genus-species">S. oralis</named-content> Subspecies, and <italic toggle="yes">S. infantis</italic>
title_sort	identification of virulence-associated properties by comparative genome analysis of <named-content content-type="genus-species">streptococcus pneumoniae</named-content>, <named-content content-type="genus-species">s. pseudopneumoniae</named-content>, <named-content content-type="genus-species">s. mitis</named-content>, three <named-content content-type="genus-species">s. oralis</named-content> subspecies, and <italic toggle="yes">s. infantis</italic>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/7af388da477d402f8d9ba062aa7524df
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