Transcriptomic Analysis of <named-content content-type="genus-species">Streptococcus pyogenes</named-content> Colonizing the Vaginal Mucosa Identifies <italic toggle="yes">hupY</italic>, an MtsR-Regulated Adhesin Involved in Heme Utilization

ABSTRACT Streptococcus pyogenes (group A streptococcus [GAS]) is a serious human pathogen with the ability to colonize mucosal surfaces such as the nasopharynx and vaginal tract, often leading to infections such as pharyngitis and vulvovaginitis. We present genome-wide transcriptome sequencing (RNAS...

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Autores principales:	Laura C. C. Cook, Nilanjana Chatterjee, Yan Li, Jorge Andrade, Michael J. Federle, Zehava Eichenbaum
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	colonization Streptococcus adherence heme iron uptake Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c6d79089914746b8b2256d0f0e6bd126
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spelling	oai:doaj.org-article:c6d79089914746b8b2256d0f0e6bd1262021-11-15T15:55:24ZTranscriptomic Analysis of <named-content content-type="genus-species">Streptococcus pyogenes</named-content> Colonizing the Vaginal Mucosa Identifies <italic toggle="yes">hupY</italic>, an MtsR-Regulated Adhesin Involved in Heme Utilization10.1128/mBio.00848-192150-7511https://doaj.org/article/c6d79089914746b8b2256d0f0e6bd1262019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00848-19https://doaj.org/toc/2150-7511ABSTRACT Streptococcus pyogenes (group A streptococcus [GAS]) is a serious human pathogen with the ability to colonize mucosal surfaces such as the nasopharynx and vaginal tract, often leading to infections such as pharyngitis and vulvovaginitis. We present genome-wide transcriptome sequencing (RNASeq) data showing the transcriptomic changes GAS undergoes during vaginal colonization. These data reveal that the regulon controlled by MtsR, a master metal regulator, is activated during vaginal colonization. This regulon includes two genes highly expressed during vaginal colonization, hupYZ. Here we show that HupY binds heme in vitro, affects intracellular concentrations of iron, and is essential for proper growth of GAS using hemoglobin or serum as the sole iron source. HupY is also important for murine vaginal colonization of both GAS and the related vaginal colonizer and pathogen Streptococcus agalactiae (group B streptococcus [GBS]). These data provide essential information on the link between metal regulation and mucosal colonization in both GAS and GBS. IMPORTANCE Colonization of the host requires the ability to adapt to an environment that is often low in essential nutrients such as iron. Here we present data showing that the transcriptome of the important human pathogen Streptococcus pyogenes shows extensive remodeling during in vivo growth, resulting in, among many other differentially expressed genes and pathways, a significant increase in genes involved in acquiring iron from host heme. Data show that HupY, previously characterized as an adhesin in both S. pyogenes and the related pathogen Streptococcus agalactiae, binds heme and affects intracellular iron concentrations. HupY, a protein with no known heme binding domains, represents a novel heme binding protein playing an important role in bacterial iron homeostasis as well as vaginal colonization.Laura C. C. CookNilanjana ChatterjeeYan LiJorge AndradeMichael J. FederleZehava EichenbaumAmerican Society for MicrobiologyarticlecolonizationStreptococcusadherencehemeiron uptakeMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	colonization Streptococcus adherence heme iron uptake Microbiology QR1-502
spellingShingle	colonization Streptococcus adherence heme iron uptake Microbiology QR1-502 Laura C. C. Cook Nilanjana Chatterjee Yan Li Jorge Andrade Michael J. Federle Zehava Eichenbaum Transcriptomic Analysis of <named-content content-type="genus-species">Streptococcus pyogenes</named-content> Colonizing the Vaginal Mucosa Identifies <italic toggle="yes">hupY</italic>, an MtsR-Regulated Adhesin Involved in Heme Utilization
description	ABSTRACT Streptococcus pyogenes (group A streptococcus [GAS]) is a serious human pathogen with the ability to colonize mucosal surfaces such as the nasopharynx and vaginal tract, often leading to infections such as pharyngitis and vulvovaginitis. We present genome-wide transcriptome sequencing (RNASeq) data showing the transcriptomic changes GAS undergoes during vaginal colonization. These data reveal that the regulon controlled by MtsR, a master metal regulator, is activated during vaginal colonization. This regulon includes two genes highly expressed during vaginal colonization, hupYZ. Here we show that HupY binds heme in vitro, affects intracellular concentrations of iron, and is essential for proper growth of GAS using hemoglobin or serum as the sole iron source. HupY is also important for murine vaginal colonization of both GAS and the related vaginal colonizer and pathogen Streptococcus agalactiae (group B streptococcus [GBS]). These data provide essential information on the link between metal regulation and mucosal colonization in both GAS and GBS. IMPORTANCE Colonization of the host requires the ability to adapt to an environment that is often low in essential nutrients such as iron. Here we present data showing that the transcriptome of the important human pathogen Streptococcus pyogenes shows extensive remodeling during in vivo growth, resulting in, among many other differentially expressed genes and pathways, a significant increase in genes involved in acquiring iron from host heme. Data show that HupY, previously characterized as an adhesin in both S. pyogenes and the related pathogen Streptococcus agalactiae, binds heme and affects intracellular iron concentrations. HupY, a protein with no known heme binding domains, represents a novel heme binding protein playing an important role in bacterial iron homeostasis as well as vaginal colonization.
format	article
author	Laura C. C. Cook Nilanjana Chatterjee Yan Li Jorge Andrade Michael J. Federle Zehava Eichenbaum
author_facet	Laura C. C. Cook Nilanjana Chatterjee Yan Li Jorge Andrade Michael J. Federle Zehava Eichenbaum
author_sort	Laura C. C. Cook
title	Transcriptomic Analysis of <named-content content-type="genus-species">Streptococcus pyogenes</named-content> Colonizing the Vaginal Mucosa Identifies <italic toggle="yes">hupY</italic>, an MtsR-Regulated Adhesin Involved in Heme Utilization
title_short	Transcriptomic Analysis of <named-content content-type="genus-species">Streptococcus pyogenes</named-content> Colonizing the Vaginal Mucosa Identifies <italic toggle="yes">hupY</italic>, an MtsR-Regulated Adhesin Involved in Heme Utilization
title_full	Transcriptomic Analysis of <named-content content-type="genus-species">Streptococcus pyogenes</named-content> Colonizing the Vaginal Mucosa Identifies <italic toggle="yes">hupY</italic>, an MtsR-Regulated Adhesin Involved in Heme Utilization
title_fullStr	Transcriptomic Analysis of <named-content content-type="genus-species">Streptococcus pyogenes</named-content> Colonizing the Vaginal Mucosa Identifies <italic toggle="yes">hupY</italic>, an MtsR-Regulated Adhesin Involved in Heme Utilization
title_full_unstemmed	Transcriptomic Analysis of <named-content content-type="genus-species">Streptococcus pyogenes</named-content> Colonizing the Vaginal Mucosa Identifies <italic toggle="yes">hupY</italic>, an MtsR-Regulated Adhesin Involved in Heme Utilization
title_sort	transcriptomic analysis of <named-content content-type="genus-species">streptococcus pyogenes</named-content> colonizing the vaginal mucosa identifies <italic toggle="yes">hupy</italic>, an mtsr-regulated adhesin involved in heme utilization
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/c6d79089914746b8b2256d0f0e6bd126
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Transcriptomic Analysis of <named-content content-type="genus-species">Streptococcus pyogenes</named-content> Colonizing the Vaginal Mucosa Identifies <italic toggle="yes">hupY</italic>, an MtsR-Regulated Adhesin Involved in Heme Utilization

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