Comparative Transcriptomic Profiling of <named-content content-type="genus-species">Yersinia enterocolitica</named-content> O:3 and O:8 Reveals Major Expression Differences of Fitness- and Virulence-Relevant Genes Indicating Ecological Separation

ABSTRACT Yersinia enterocolitica is a zoonotic pathogen and an important cause of bacterial gastrointestinal infections in humans. Large-scale population genomic analyses revealed genetic and phenotypic diversity of this bacterial species, but little is known about the differences in the transcripto...

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Autores principales:	Carina Schmühl, Michael Beckstette, Ann Kathrin Heroven, Boyke Bunk, Cathrin Spröer, Alan McNally, Jörg Overmann, Petra Dersch
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Yersinia enterocolitica YstA toxin comparative transcriptomics growth-phase control temperature regulation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d2de501bb5814625ad140b0be65344b0
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spelling	oai:doaj.org-article:d2de501bb5814625ad140b0be65344b02021-12-02T19:46:17ZComparative Transcriptomic Profiling of <named-content content-type="genus-species">Yersinia enterocolitica</named-content> O:3 and O:8 Reveals Major Expression Differences of Fitness- and Virulence-Relevant Genes Indicating Ecological Separation10.1128/mSystems.00239-182379-5077https://doaj.org/article/d2de501bb5814625ad140b0be65344b02019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00239-18https://doaj.org/toc/2379-5077ABSTRACT Yersinia enterocolitica is a zoonotic pathogen and an important cause of bacterial gastrointestinal infections in humans. Large-scale population genomic analyses revealed genetic and phenotypic diversity of this bacterial species, but little is known about the differences in the transcriptome organization, small RNA (sRNA) repertoire, and transcriptional output. Here, we present the first comparative high-resolution transcriptome analysis of Y. enterocolitica strains representing highly pathogenic phylogroup 2 (serotype O:8) and moderately pathogenic phylogroup 3 (serotype O:3) grown under four infection-relevant conditions. Our transcriptome sequencing (RNA-seq) approach revealed 1,299 and 1,076 transcriptional start sites and identified strain-specific sRNAs that could contribute to differential regulation among the phylogroups. Comparative transcriptomics further uncovered major gene expression differences, in particular, in the temperature-responsive regulon. Multiple virulence-relevant genes are differentially regulated between the two strains, supporting an ecological separation of phylogroups with certain niche-adapted properties. Strong upregulation of the ystA enterotoxin gene in combination with constitutive high expression of cell invasion factor InvA further showed that the toxicity of recent outbreak O:3 strains has increased. Overall, our report provides new insights into the specific transcriptome organization of phylogroups 2 and 3 and reveals gene expression differences contributing to the substantial phenotypic differences that exist between the lineages. IMPORTANCE Yersinia enterocolitica is a major diarrheal pathogen and is associated with a large range of gut-associated diseases. Members of this species have evolved into different phylogroups with genotypic variations. We performed the first characterization of the Y. enterocolitica transcriptional landscape and tracked the consequences of the genomic variations between two different pathogenic phylogroups by comparing their RNA repertoire, promoter usage, and expression profiles under four different virulence-relevant conditions. Our analysis revealed major differences in the transcriptional outputs of the closely related strains, pointing to an ecological separation in which one is more adapted to an environmental lifestyle and the other to a mostly mammal-associated lifestyle. Moreover, a variety of pathoadaptive alterations, including alterations in acid resistance genes, colonization factors, and toxins, were identified which affect virulence and host specificity. This illustrates that comparative transcriptomics is an excellent approach to discover differences in the functional output from closely related genomes affecting niche adaptation and virulence, which cannot be directly inferred from DNA sequences.Carina SchmühlMichael BeckstetteAnn Kathrin HerovenBoyke BunkCathrin SpröerAlan McNallyJörg OvermannPetra DerschAmerican Society for MicrobiologyarticleYersinia enterocoliticaYstA toxincomparative transcriptomicsgrowth-phase controltemperature regulationMicrobiologyQR1-502ENmSystems, Vol 4, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Yersinia enterocolitica YstA toxin comparative transcriptomics growth-phase control temperature regulation Microbiology QR1-502
spellingShingle	Yersinia enterocolitica YstA toxin comparative transcriptomics growth-phase control temperature regulation Microbiology QR1-502 Carina Schmühl Michael Beckstette Ann Kathrin Heroven Boyke Bunk Cathrin Spröer Alan McNally Jörg Overmann Petra Dersch Comparative Transcriptomic Profiling of <named-content content-type="genus-species">Yersinia enterocolitica</named-content> O:3 and O:8 Reveals Major Expression Differences of Fitness- and Virulence-Relevant Genes Indicating Ecological Separation
description	ABSTRACT Yersinia enterocolitica is a zoonotic pathogen and an important cause of bacterial gastrointestinal infections in humans. Large-scale population genomic analyses revealed genetic and phenotypic diversity of this bacterial species, but little is known about the differences in the transcriptome organization, small RNA (sRNA) repertoire, and transcriptional output. Here, we present the first comparative high-resolution transcriptome analysis of Y. enterocolitica strains representing highly pathogenic phylogroup 2 (serotype O:8) and moderately pathogenic phylogroup 3 (serotype O:3) grown under four infection-relevant conditions. Our transcriptome sequencing (RNA-seq) approach revealed 1,299 and 1,076 transcriptional start sites and identified strain-specific sRNAs that could contribute to differential regulation among the phylogroups. Comparative transcriptomics further uncovered major gene expression differences, in particular, in the temperature-responsive regulon. Multiple virulence-relevant genes are differentially regulated between the two strains, supporting an ecological separation of phylogroups with certain niche-adapted properties. Strong upregulation of the ystA enterotoxin gene in combination with constitutive high expression of cell invasion factor InvA further showed that the toxicity of recent outbreak O:3 strains has increased. Overall, our report provides new insights into the specific transcriptome organization of phylogroups 2 and 3 and reveals gene expression differences contributing to the substantial phenotypic differences that exist between the lineages. IMPORTANCE Yersinia enterocolitica is a major diarrheal pathogen and is associated with a large range of gut-associated diseases. Members of this species have evolved into different phylogroups with genotypic variations. We performed the first characterization of the Y. enterocolitica transcriptional landscape and tracked the consequences of the genomic variations between two different pathogenic phylogroups by comparing their RNA repertoire, promoter usage, and expression profiles under four different virulence-relevant conditions. Our analysis revealed major differences in the transcriptional outputs of the closely related strains, pointing to an ecological separation in which one is more adapted to an environmental lifestyle and the other to a mostly mammal-associated lifestyle. Moreover, a variety of pathoadaptive alterations, including alterations in acid resistance genes, colonization factors, and toxins, were identified which affect virulence and host specificity. This illustrates that comparative transcriptomics is an excellent approach to discover differences in the functional output from closely related genomes affecting niche adaptation and virulence, which cannot be directly inferred from DNA sequences.
format	article
author	Carina Schmühl Michael Beckstette Ann Kathrin Heroven Boyke Bunk Cathrin Spröer Alan McNally Jörg Overmann Petra Dersch
author_facet	Carina Schmühl Michael Beckstette Ann Kathrin Heroven Boyke Bunk Cathrin Spröer Alan McNally Jörg Overmann Petra Dersch
author_sort	Carina Schmühl
title	Comparative Transcriptomic Profiling of <named-content content-type="genus-species">Yersinia enterocolitica</named-content> O:3 and O:8 Reveals Major Expression Differences of Fitness- and Virulence-Relevant Genes Indicating Ecological Separation
title_short	Comparative Transcriptomic Profiling of <named-content content-type="genus-species">Yersinia enterocolitica</named-content> O:3 and O:8 Reveals Major Expression Differences of Fitness- and Virulence-Relevant Genes Indicating Ecological Separation
title_full	Comparative Transcriptomic Profiling of <named-content content-type="genus-species">Yersinia enterocolitica</named-content> O:3 and O:8 Reveals Major Expression Differences of Fitness- and Virulence-Relevant Genes Indicating Ecological Separation
title_fullStr	Comparative Transcriptomic Profiling of <named-content content-type="genus-species">Yersinia enterocolitica</named-content> O:3 and O:8 Reveals Major Expression Differences of Fitness- and Virulence-Relevant Genes Indicating Ecological Separation
title_full_unstemmed	Comparative Transcriptomic Profiling of <named-content content-type="genus-species">Yersinia enterocolitica</named-content> O:3 and O:8 Reveals Major Expression Differences of Fitness- and Virulence-Relevant Genes Indicating Ecological Separation
title_sort	comparative transcriptomic profiling of <named-content content-type="genus-species">yersinia enterocolitica</named-content> o:3 and o:8 reveals major expression differences of fitness- and virulence-relevant genes indicating ecological separation
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/d2de501bb5814625ad140b0be65344b0
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Comparative Transcriptomic Profiling of <named-content content-type="genus-species">Yersinia enterocolitica</named-content> O:3 and O:8 Reveals Major Expression Differences of Fitness- and Virulence-Relevant Genes Indicating Ecological Separation

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