Parallel Evolution of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and <named-content content-type="genus-species">Streptococcus mitis</named-content> to Pathogenic and Mutualistic Lifestyles

ABSTRACT The bacterium Streptococcus pneumoniae is one of the leading causes of fatal infections affecting humans. Intriguingly, phylogenetic analysis shows that the species constitutes one evolutionary lineage in a cluster of the otherwise commensal Streptococcus mitis strains, with which humans li...

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Autores principales:	Mogens Kilian, David R. Riley, Anders Jensen, Holger Brüggemann, Hervé Tettelin
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/df7f223bed8a4bc1beb63d1f377998a1
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spelling	oai:doaj.org-article:df7f223bed8a4bc1beb63d1f377998a12021-11-15T15:47:21ZParallel Evolution of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and <named-content content-type="genus-species">Streptococcus mitis</named-content> to Pathogenic and Mutualistic Lifestyles10.1128/mBio.01490-142150-7511https://doaj.org/article/df7f223bed8a4bc1beb63d1f377998a12014-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01490-14https://doaj.org/toc/2150-7511ABSTRACT The bacterium Streptococcus pneumoniae is one of the leading causes of fatal infections affecting humans. Intriguingly, phylogenetic analysis shows that the species constitutes one evolutionary lineage in a cluster of the otherwise commensal Streptococcus mitis strains, with which humans live in harmony. In a comparative analysis of 35 genomes, including phylogenetic analyses of all predicted genes, we have shown that the pathogenic pneumococcus has evolved into a master of genomic flexibility while lineages that evolved into the nonpathogenic S. mitis secured harmonious coexistence with their host by stabilizing an approximately 15%-reduced genome devoid of many virulence genes. Our data further provide evidence that interspecies gene transfer between S. pneumoniae and S. mitis occurs in a unidirectional manner, i.e., from S. mitis to S. pneumoniae. Import of genes from S. mitis and other mitis, anginosus, and salivarius group streptococci ensured allelic replacements and antigenic diversification and has been driving the evolution of the remarkable structural diversity of capsular polysaccharides of S. pneumoniae. Our study explains how the unique structural diversity of the pneumococcal capsule emerged and conceivably will continue to increase and reveals a striking example of the fragile border between the commensal and pathogenic lifestyles. While genomic plasticity enabling quick adaptation to environmental stress is a necessity for the pathogenic streptococci, the commensal lifestyle benefits from stability. IMPORTANCE One of the leading causes of fatal infections affecting humans, Streptococcus pneumoniae, and the commensal Streptococcus mitis are closely related obligate symbionts associated with hominids. Faced with a shortage of accessible hosts, the two opposing lifestyles evolved in parallel. We have shown that the nonpathogenic S. mitis secured harmonious coexistence with its host by stabilizing a reduced genome devoid of many virulence genes. Meanwhile, the pathogenic pneumococcus evolved into a master of genomic flexibility and imports genes from S. mitis and other related streptococci. This process ensured antigenic diversification and has been driving the evolution of the remarkable structural diversity of capsular polysaccharides of S. pneumoniae, which conceivably will continue to increase and present a challenge to disease prevention.Mogens KilianDavid R. RileyAnders JensenHolger BrüggemannHervé TettelinAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 4 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Mogens Kilian David R. Riley Anders Jensen Holger Brüggemann Hervé Tettelin Parallel Evolution of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and <named-content content-type="genus-species">Streptococcus mitis</named-content> to Pathogenic and Mutualistic Lifestyles
description	ABSTRACT The bacterium Streptococcus pneumoniae is one of the leading causes of fatal infections affecting humans. Intriguingly, phylogenetic analysis shows that the species constitutes one evolutionary lineage in a cluster of the otherwise commensal Streptococcus mitis strains, with which humans live in harmony. In a comparative analysis of 35 genomes, including phylogenetic analyses of all predicted genes, we have shown that the pathogenic pneumococcus has evolved into a master of genomic flexibility while lineages that evolved into the nonpathogenic S. mitis secured harmonious coexistence with their host by stabilizing an approximately 15%-reduced genome devoid of many virulence genes. Our data further provide evidence that interspecies gene transfer between S. pneumoniae and S. mitis occurs in a unidirectional manner, i.e., from S. mitis to S. pneumoniae. Import of genes from S. mitis and other mitis, anginosus, and salivarius group streptococci ensured allelic replacements and antigenic diversification and has been driving the evolution of the remarkable structural diversity of capsular polysaccharides of S. pneumoniae. Our study explains how the unique structural diversity of the pneumococcal capsule emerged and conceivably will continue to increase and reveals a striking example of the fragile border between the commensal and pathogenic lifestyles. While genomic plasticity enabling quick adaptation to environmental stress is a necessity for the pathogenic streptococci, the commensal lifestyle benefits from stability. IMPORTANCE One of the leading causes of fatal infections affecting humans, Streptococcus pneumoniae, and the commensal Streptococcus mitis are closely related obligate symbionts associated with hominids. Faced with a shortage of accessible hosts, the two opposing lifestyles evolved in parallel. We have shown that the nonpathogenic S. mitis secured harmonious coexistence with its host by stabilizing a reduced genome devoid of many virulence genes. Meanwhile, the pathogenic pneumococcus evolved into a master of genomic flexibility and imports genes from S. mitis and other related streptococci. This process ensured antigenic diversification and has been driving the evolution of the remarkable structural diversity of capsular polysaccharides of S. pneumoniae, which conceivably will continue to increase and present a challenge to disease prevention.
format	article
author	Mogens Kilian David R. Riley Anders Jensen Holger Brüggemann Hervé Tettelin
author_facet	Mogens Kilian David R. Riley Anders Jensen Holger Brüggemann Hervé Tettelin
author_sort	Mogens Kilian
title	Parallel Evolution of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and <named-content content-type="genus-species">Streptococcus mitis</named-content> to Pathogenic and Mutualistic Lifestyles
title_short	Parallel Evolution of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and <named-content content-type="genus-species">Streptococcus mitis</named-content> to Pathogenic and Mutualistic Lifestyles
title_full	Parallel Evolution of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and <named-content content-type="genus-species">Streptococcus mitis</named-content> to Pathogenic and Mutualistic Lifestyles
title_fullStr	Parallel Evolution of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and <named-content content-type="genus-species">Streptococcus mitis</named-content> to Pathogenic and Mutualistic Lifestyles
title_full_unstemmed	Parallel Evolution of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and <named-content content-type="genus-species">Streptococcus mitis</named-content> to Pathogenic and Mutualistic Lifestyles
title_sort	parallel evolution of <named-content content-type="genus-species">streptococcus pneumoniae</named-content> and <named-content content-type="genus-species">streptococcus mitis</named-content> to pathogenic and mutualistic lifestyles
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/df7f223bed8a4bc1beb63d1f377998a1
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Parallel Evolution of <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and <named-content content-type="genus-species">Streptococcus mitis</named-content> to Pathogenic and Mutualistic Lifestyles

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