Parallel Evolution of Group B <italic toggle="yes">Streptococcus</italic> Hypervirulent Clonal Complex 17 Unveils New Pathoadaptive Mutations

ABSTRACT Group B Streptococcus (GBS) is a commensal of the gastrointestinal and genitourinary tracts, while a prevailing cause of neonatal disease worldwide. Of the various clonal complexes (CCs), CC17 is overrepresented in GBS-infected newborns for reasons that are still largely unknown. Here, we r...

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Autores principales:	Alexandre Almeida, Isabelle Rosinski-Chupin, Céline Plainvert, Pierre-Emmanuel Douarre, Maria J. Borrego, Claire Poyart, Philippe Glaser
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	CovR ST17 antibiotic resistance eubacteria evolution genomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4efc896ebfa747b98af92dbf286cd486
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spelling	oai:doaj.org-article:4efc896ebfa747b98af92dbf286cd4862021-12-02T19:45:29ZParallel Evolution of Group B <italic toggle="yes">Streptococcus</italic> Hypervirulent Clonal Complex 17 Unveils New Pathoadaptive Mutations10.1128/mSystems.00074-172379-5077https://doaj.org/article/4efc896ebfa747b98af92dbf286cd4862017-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00074-17https://doaj.org/toc/2379-5077ABSTRACT Group B Streptococcus (GBS) is a commensal of the gastrointestinal and genitourinary tracts, while a prevailing cause of neonatal disease worldwide. Of the various clonal complexes (CCs), CC17 is overrepresented in GBS-infected newborns for reasons that are still largely unknown. Here, we report a comprehensive genomic analysis of 626 CC17 isolates collected worldwide, identifying the genetic traits behind their successful adaptation to humans and the underlying differences between carriage and clinical strains. Comparative analysis with 923 GBS genomes belonging to CC1, CC19, and CC23 revealed that the evolution of CC17 is distinct from that of other human-adapted lineages and recurrently targets functions related to nucleotide and amino acid metabolism, cell adhesion, regulation, and immune evasion. We show that the most distinctive features of disease-specific CC17 isolates were frequent mutations in the virulence-associated CovS and Stk1 kinases, underscoring the crucial role of the entire CovRS regulatory pathway in modulating the pathogenicity of GBS. Importantly, parallel and convergent evolution of major components of the bacterial cell envelope, such as the capsule biosynthesis operon, the pilus, and Rib, reflects adaptation to host immune pressures and should be taken into account in the ongoing development of a GBS vaccine. The presence of recurrent targets of evolution not previously implicated in virulence also opens the way for uncovering new functions involved in host colonization and GBS pathogenesis. IMPORTANCE The incidence of group B Streptococcus (GBS) neonatal disease continues to be a significant cause of concern worldwide. Strains belonging to clonal complex 17 (CC17) are the most frequently responsible for GBS infections in neonates, especially among late-onset disease cases. Therefore, we undertook the largest genomic study of GBS CC17 strains to date to decipher the genetic bases of their remarkable colonization and infection ability. We show that crucial functions involved in different steps of the colonization or infection process of GBS are distinctly mutated during the adaptation of CC17 to the human host. In particular, our results implicate the CovRS two-component regulator of virulence in the differentiation between carriage- and disease-associated isolates. Not only does this work raise important implications for the ongoing development of a vaccine against GBS but might also drive the discovery of key functions for GBS adaptation and pathogenesis that have been overlooked until now. Author Video: An author video summary of this article is available.Alexandre AlmeidaIsabelle Rosinski-ChupinCéline PlainvertPierre-Emmanuel DouarreMaria J. BorregoClaire PoyartPhilippe GlaserAmerican Society for MicrobiologyarticleCovRST17antibiotic resistanceeubacteriaevolutiongenomicsMicrobiologyQR1-502ENmSystems, Vol 2, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	CovR ST17 antibiotic resistance eubacteria evolution genomics Microbiology QR1-502
spellingShingle	CovR ST17 antibiotic resistance eubacteria evolution genomics Microbiology QR1-502 Alexandre Almeida Isabelle Rosinski-Chupin Céline Plainvert Pierre-Emmanuel Douarre Maria J. Borrego Claire Poyart Philippe Glaser Parallel Evolution of Group B <italic toggle="yes">Streptococcus</italic> Hypervirulent Clonal Complex 17 Unveils New Pathoadaptive Mutations
description	ABSTRACT Group B Streptococcus (GBS) is a commensal of the gastrointestinal and genitourinary tracts, while a prevailing cause of neonatal disease worldwide. Of the various clonal complexes (CCs), CC17 is overrepresented in GBS-infected newborns for reasons that are still largely unknown. Here, we report a comprehensive genomic analysis of 626 CC17 isolates collected worldwide, identifying the genetic traits behind their successful adaptation to humans and the underlying differences between carriage and clinical strains. Comparative analysis with 923 GBS genomes belonging to CC1, CC19, and CC23 revealed that the evolution of CC17 is distinct from that of other human-adapted lineages and recurrently targets functions related to nucleotide and amino acid metabolism, cell adhesion, regulation, and immune evasion. We show that the most distinctive features of disease-specific CC17 isolates were frequent mutations in the virulence-associated CovS and Stk1 kinases, underscoring the crucial role of the entire CovRS regulatory pathway in modulating the pathogenicity of GBS. Importantly, parallel and convergent evolution of major components of the bacterial cell envelope, such as the capsule biosynthesis operon, the pilus, and Rib, reflects adaptation to host immune pressures and should be taken into account in the ongoing development of a GBS vaccine. The presence of recurrent targets of evolution not previously implicated in virulence also opens the way for uncovering new functions involved in host colonization and GBS pathogenesis. IMPORTANCE The incidence of group B Streptococcus (GBS) neonatal disease continues to be a significant cause of concern worldwide. Strains belonging to clonal complex 17 (CC17) are the most frequently responsible for GBS infections in neonates, especially among late-onset disease cases. Therefore, we undertook the largest genomic study of GBS CC17 strains to date to decipher the genetic bases of their remarkable colonization and infection ability. We show that crucial functions involved in different steps of the colonization or infection process of GBS are distinctly mutated during the adaptation of CC17 to the human host. In particular, our results implicate the CovRS two-component regulator of virulence in the differentiation between carriage- and disease-associated isolates. Not only does this work raise important implications for the ongoing development of a vaccine against GBS but might also drive the discovery of key functions for GBS adaptation and pathogenesis that have been overlooked until now. Author Video: An author video summary of this article is available.
format	article
author	Alexandre Almeida Isabelle Rosinski-Chupin Céline Plainvert Pierre-Emmanuel Douarre Maria J. Borrego Claire Poyart Philippe Glaser
author_facet	Alexandre Almeida Isabelle Rosinski-Chupin Céline Plainvert Pierre-Emmanuel Douarre Maria J. Borrego Claire Poyart Philippe Glaser
author_sort	Alexandre Almeida
title	Parallel Evolution of Group B <italic toggle="yes">Streptococcus</italic> Hypervirulent Clonal Complex 17 Unveils New Pathoadaptive Mutations
title_short	Parallel Evolution of Group B <italic toggle="yes">Streptococcus</italic> Hypervirulent Clonal Complex 17 Unveils New Pathoadaptive Mutations
title_full	Parallel Evolution of Group B <italic toggle="yes">Streptococcus</italic> Hypervirulent Clonal Complex 17 Unveils New Pathoadaptive Mutations
title_fullStr	Parallel Evolution of Group B <italic toggle="yes">Streptococcus</italic> Hypervirulent Clonal Complex 17 Unveils New Pathoadaptive Mutations
title_full_unstemmed	Parallel Evolution of Group B <italic toggle="yes">Streptococcus</italic> Hypervirulent Clonal Complex 17 Unveils New Pathoadaptive Mutations
title_sort	parallel evolution of group b <italic toggle="yes">streptococcus</italic> hypervirulent clonal complex 17 unveils new pathoadaptive mutations
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/4efc896ebfa747b98af92dbf286cd486
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Parallel Evolution of Group B <italic toggle="yes">Streptococcus</italic> Hypervirulent Clonal Complex 17 Unveils New Pathoadaptive Mutations

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