Differential Gene Expression Patterns of <italic toggle="yes">Yersinia pestis</italic> and <italic toggle="yes">Yersinia pseudotuberculosis</italic> during Infection and Biofilm Formation in the Flea Digestive Tract

ABSTRACT Yersinia pestis, the etiologic agent of plague, emerged as a fleaborne pathogen only within the last 6,000 years. Just five simple genetic changes in the Yersinia pseudotuberculosis progenitor, which served to eliminate toxicity to fleas and to enhance survival and biofilm formation in the...

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Autores principales:	Iman Chouikha, Daniel E. Sturdevant, Clayton Jarrett, Yi-Cheng Sun, B. Joseph Hinnebusch
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Yersinia pestis Yersinia pseudotuberculosis arthropodborne transmission biofilm flea plague Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/1809ebbe8abc485e9e0623bf13242ff2
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spelling	oai:doaj.org-article:1809ebbe8abc485e9e0623bf13242ff22021-12-02T19:46:18ZDifferential Gene Expression Patterns of <italic toggle="yes">Yersinia pestis</italic> and <italic toggle="yes">Yersinia pseudotuberculosis</italic> during Infection and Biofilm Formation in the Flea Digestive Tract10.1128/mSystems.00217-182379-5077https://doaj.org/article/1809ebbe8abc485e9e0623bf13242ff22019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00217-18https://doaj.org/toc/2379-5077ABSTRACT Yersinia pestis, the etiologic agent of plague, emerged as a fleaborne pathogen only within the last 6,000 years. Just five simple genetic changes in the Yersinia pseudotuberculosis progenitor, which served to eliminate toxicity to fleas and to enhance survival and biofilm formation in the flea digestive tract, were key to the transition to the arthropodborne transmission route. To gain a deeper understanding of the genetic basis for the development of a transmissible biofilm infection in the flea foregut, we evaluated additional gene differences and performed in vivo transcriptional profiling of Y. pestis, a Y. pseudotuberculosis wild-type strain (unable to form biofilm in the flea foregut), and a Y. pseudotuberculosis mutant strain (able to produce foregut-blocking biofilm in fleas) recovered from fleas 1 day and 14 days after an infectious blood meal. Surprisingly, the Y. pseudotuberculosis mutations that increased c-di-GMP levels and enabled biofilm development in the flea did not change the expression levels of the hms genes responsible for the synthesis and export of the extracellular polysaccharide matrix required for mature biofilm formation. The Y. pseudotuberculosis mutant uniquely expressed much higher levels of Yersinia type VI secretion system 4 (T6SS-4) in the flea, and this locus was required for flea blockage by Y. pseudotuberculosis but not for blockage by Y. pestis. Significant differences between the two species in expression of several metabolism genes, the Psa fimbrial genes, quorum sensing-related genes, transcription regulation genes, and stress response genes were evident during flea infection. IMPORTANCE Y. pestis emerged as a highly virulent, arthropod-transmitted pathogen on the basis of relatively few and discrete genetic changes from Y. pseudotuberculosis. Parallel comparisons of the in vitro and in vivo transcriptomes of Y. pestis and two Y. pseudotuberculosis variants that produce a nontransmissible infection and a transmissible infection of the flea vector, respectively, provided insights into how Y. pestis has adapted to life in its flea vector and point to evolutionary changes in the regulation of metabolic and biofilm development pathways in these two closely related species.Iman ChouikhaDaniel E. SturdevantClayton JarrettYi-Cheng SunB. Joseph HinnebuschAmerican Society for MicrobiologyarticleYersinia pestisYersinia pseudotuberculosisarthropodborne transmissionbiofilmfleaplagueMicrobiologyQR1-502ENmSystems, Vol 4, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Yersinia pestis Yersinia pseudotuberculosis arthropodborne transmission biofilm flea plague Microbiology QR1-502
spellingShingle	Yersinia pestis Yersinia pseudotuberculosis arthropodborne transmission biofilm flea plague Microbiology QR1-502 Iman Chouikha Daniel E. Sturdevant Clayton Jarrett Yi-Cheng Sun B. Joseph Hinnebusch Differential Gene Expression Patterns of <italic toggle="yes">Yersinia pestis</italic> and <italic toggle="yes">Yersinia pseudotuberculosis</italic> during Infection and Biofilm Formation in the Flea Digestive Tract
description	ABSTRACT Yersinia pestis, the etiologic agent of plague, emerged as a fleaborne pathogen only within the last 6,000 years. Just five simple genetic changes in the Yersinia pseudotuberculosis progenitor, which served to eliminate toxicity to fleas and to enhance survival and biofilm formation in the flea digestive tract, were key to the transition to the arthropodborne transmission route. To gain a deeper understanding of the genetic basis for the development of a transmissible biofilm infection in the flea foregut, we evaluated additional gene differences and performed in vivo transcriptional profiling of Y. pestis, a Y. pseudotuberculosis wild-type strain (unable to form biofilm in the flea foregut), and a Y. pseudotuberculosis mutant strain (able to produce foregut-blocking biofilm in fleas) recovered from fleas 1 day and 14 days after an infectious blood meal. Surprisingly, the Y. pseudotuberculosis mutations that increased c-di-GMP levels and enabled biofilm development in the flea did not change the expression levels of the hms genes responsible for the synthesis and export of the extracellular polysaccharide matrix required for mature biofilm formation. The Y. pseudotuberculosis mutant uniquely expressed much higher levels of Yersinia type VI secretion system 4 (T6SS-4) in the flea, and this locus was required for flea blockage by Y. pseudotuberculosis but not for blockage by Y. pestis. Significant differences between the two species in expression of several metabolism genes, the Psa fimbrial genes, quorum sensing-related genes, transcription regulation genes, and stress response genes were evident during flea infection. IMPORTANCE Y. pestis emerged as a highly virulent, arthropod-transmitted pathogen on the basis of relatively few and discrete genetic changes from Y. pseudotuberculosis. Parallel comparisons of the in vitro and in vivo transcriptomes of Y. pestis and two Y. pseudotuberculosis variants that produce a nontransmissible infection and a transmissible infection of the flea vector, respectively, provided insights into how Y. pestis has adapted to life in its flea vector and point to evolutionary changes in the regulation of metabolic and biofilm development pathways in these two closely related species.
format	article
author	Iman Chouikha Daniel E. Sturdevant Clayton Jarrett Yi-Cheng Sun B. Joseph Hinnebusch
author_facet	Iman Chouikha Daniel E. Sturdevant Clayton Jarrett Yi-Cheng Sun B. Joseph Hinnebusch
author_sort	Iman Chouikha
title	Differential Gene Expression Patterns of <italic toggle="yes">Yersinia pestis</italic> and <italic toggle="yes">Yersinia pseudotuberculosis</italic> during Infection and Biofilm Formation in the Flea Digestive Tract
title_short	Differential Gene Expression Patterns of <italic toggle="yes">Yersinia pestis</italic> and <italic toggle="yes">Yersinia pseudotuberculosis</italic> during Infection and Biofilm Formation in the Flea Digestive Tract
title_full	Differential Gene Expression Patterns of <italic toggle="yes">Yersinia pestis</italic> and <italic toggle="yes">Yersinia pseudotuberculosis</italic> during Infection and Biofilm Formation in the Flea Digestive Tract
title_fullStr	Differential Gene Expression Patterns of <italic toggle="yes">Yersinia pestis</italic> and <italic toggle="yes">Yersinia pseudotuberculosis</italic> during Infection and Biofilm Formation in the Flea Digestive Tract
title_full_unstemmed	Differential Gene Expression Patterns of <italic toggle="yes">Yersinia pestis</italic> and <italic toggle="yes">Yersinia pseudotuberculosis</italic> during Infection and Biofilm Formation in the Flea Digestive Tract
title_sort	differential gene expression patterns of <italic toggle="yes">yersinia pestis</italic> and <italic toggle="yes">yersinia pseudotuberculosis</italic> during infection and biofilm formation in the flea digestive tract
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/1809ebbe8abc485e9e0623bf13242ff2
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Differential Gene Expression Patterns of <italic toggle="yes">Yersinia pestis</italic> and <italic toggle="yes">Yersinia pseudotuberculosis</italic> during Infection and Biofilm Formation in the Flea Digestive Tract

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