OsdR of <named-content content-type="genus-species">Streptomyces coelicolor</named-content> and the Dormancy Regulator DevR of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content> Control Overlapping Regulons

ABSTRACT Two-component regulatory systems allow bacteria to respond adequately to changes in their environment. In response to a given stimulus, a sensory kinase activates its cognate response regulator via reversible phosphorylation. The response regulator DevR activates a state of dormancy under h...

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Autores principales:	Mia Urem, Teunke van Rossum, Giselda Bucca, Geri F. Moolenaar, Emma Laing, Magda A. Świątek-Połatyńska, Joost Willemse, Elodie Tenconi, Sébastien Rigali, Nora Goosen, Colin P. Smith, Gilles P. van Wezel
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Developmental control Streptomyces dormancy stress response Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d0d85a81b67a4222a27d115c79c8e771
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spelling	oai:doaj.org-article:d0d85a81b67a4222a27d115c79c8e7712021-12-02T18:39:34ZOsdR of <named-content content-type="genus-species">Streptomyces coelicolor</named-content> and the Dormancy Regulator DevR of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content> Control Overlapping Regulons10.1128/mSystems.00014-162379-5077https://doaj.org/article/d0d85a81b67a4222a27d115c79c8e7712016-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00014-16https://doaj.org/toc/2379-5077ABSTRACT Two-component regulatory systems allow bacteria to respond adequately to changes in their environment. In response to a given stimulus, a sensory kinase activates its cognate response regulator via reversible phosphorylation. The response regulator DevR activates a state of dormancy under hypoxia in Mycobacterium tuberculosis, allowing this pathogen to escape the host defense system. Here, we show that OsdR (SCO0204) of the soil bacterium Streptomyces coelicolor is a functional orthologue of DevR. OsdR, when activated by the sensory kinase OsdK (SCO0203), binds upstream of the DevR-controlled dormancy genes devR, hspX, and Rv3134c of M. tuberculosis. In silico analysis of the S. coelicolor genome combined with in vitro DNA binding studies identified many binding sites in the genomic region around osdR itself and upstream of stress-related genes. This binding correlated well with transcriptomic responses, with deregulation of developmental genes and genes related to stress and hypoxia in the osdR mutant. A peak in osdR transcription in the wild-type strain at the onset of aerial growth correlated with major changes in global gene expression. Taken together, our data reveal the existence of a dormancy-related regulon in streptomycetes which plays an important role in the transcriptional control of stress- and development-related genes. IMPORTANCE Dormancy is a state of growth cessation that allows bacteria to escape the host defense system and antibiotic challenge. Understanding the mechanisms that control dormancy is of key importance for the treatment of latent infections, such as those from Mycobacterium tuberculosis. In mycobacteria, dormancy is controlled by the response regulator DevR, which responds to conditions of hypoxia. Here, we show that OsdR of Streptomyces coelicolor recognizes the same regulatory element and controls a regulon that consists of genes involved in the control of stress and development. Only the core regulon in the direct vicinity of dosR and osdR is conserved between M. tuberculosis and S. coelicolor, respectively. Thus, we show how the system has diverged from allowing escape from the host defense system by mycobacteria to the control of sporulation by complex multicellular streptomycetes. This provides novel insights into how bacterial growth and development are coordinated with the environmental conditions.Mia UremTeunke van RossumGiselda BuccaGeri F. MoolenaarEmma LaingMagda A. Świątek-PołatyńskaJoost WillemseElodie TenconiSébastien RigaliNora GoosenColin P. SmithGilles P. van WezelAmerican Society for MicrobiologyarticleDevelopmental controlStreptomycesdormancystress responseMicrobiologyQR1-502ENmSystems, Vol 1, Iss 3 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Developmental control Streptomyces dormancy stress response Microbiology QR1-502
spellingShingle	Developmental control Streptomyces dormancy stress response Microbiology QR1-502 Mia Urem Teunke van Rossum Giselda Bucca Geri F. Moolenaar Emma Laing Magda A. Świątek-Połatyńska Joost Willemse Elodie Tenconi Sébastien Rigali Nora Goosen Colin P. Smith Gilles P. van Wezel OsdR of <named-content content-type="genus-species">Streptomyces coelicolor</named-content> and the Dormancy Regulator DevR of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content> Control Overlapping Regulons
description	ABSTRACT Two-component regulatory systems allow bacteria to respond adequately to changes in their environment. In response to a given stimulus, a sensory kinase activates its cognate response regulator via reversible phosphorylation. The response regulator DevR activates a state of dormancy under hypoxia in Mycobacterium tuberculosis, allowing this pathogen to escape the host defense system. Here, we show that OsdR (SCO0204) of the soil bacterium Streptomyces coelicolor is a functional orthologue of DevR. OsdR, when activated by the sensory kinase OsdK (SCO0203), binds upstream of the DevR-controlled dormancy genes devR, hspX, and Rv3134c of M. tuberculosis. In silico analysis of the S. coelicolor genome combined with in vitro DNA binding studies identified many binding sites in the genomic region around osdR itself and upstream of stress-related genes. This binding correlated well with transcriptomic responses, with deregulation of developmental genes and genes related to stress and hypoxia in the osdR mutant. A peak in osdR transcription in the wild-type strain at the onset of aerial growth correlated with major changes in global gene expression. Taken together, our data reveal the existence of a dormancy-related regulon in streptomycetes which plays an important role in the transcriptional control of stress- and development-related genes. IMPORTANCE Dormancy is a state of growth cessation that allows bacteria to escape the host defense system and antibiotic challenge. Understanding the mechanisms that control dormancy is of key importance for the treatment of latent infections, such as those from Mycobacterium tuberculosis. In mycobacteria, dormancy is controlled by the response regulator DevR, which responds to conditions of hypoxia. Here, we show that OsdR of Streptomyces coelicolor recognizes the same regulatory element and controls a regulon that consists of genes involved in the control of stress and development. Only the core regulon in the direct vicinity of dosR and osdR is conserved between M. tuberculosis and S. coelicolor, respectively. Thus, we show how the system has diverged from allowing escape from the host defense system by mycobacteria to the control of sporulation by complex multicellular streptomycetes. This provides novel insights into how bacterial growth and development are coordinated with the environmental conditions.
format	article
author	Mia Urem Teunke van Rossum Giselda Bucca Geri F. Moolenaar Emma Laing Magda A. Świątek-Połatyńska Joost Willemse Elodie Tenconi Sébastien Rigali Nora Goosen Colin P. Smith Gilles P. van Wezel
author_facet	Mia Urem Teunke van Rossum Giselda Bucca Geri F. Moolenaar Emma Laing Magda A. Świątek-Połatyńska Joost Willemse Elodie Tenconi Sébastien Rigali Nora Goosen Colin P. Smith Gilles P. van Wezel
author_sort	Mia Urem
title	OsdR of <named-content content-type="genus-species">Streptomyces coelicolor</named-content> and the Dormancy Regulator DevR of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content> Control Overlapping Regulons
title_short	OsdR of <named-content content-type="genus-species">Streptomyces coelicolor</named-content> and the Dormancy Regulator DevR of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content> Control Overlapping Regulons
title_full	OsdR of <named-content content-type="genus-species">Streptomyces coelicolor</named-content> and the Dormancy Regulator DevR of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content> Control Overlapping Regulons
title_fullStr	OsdR of <named-content content-type="genus-species">Streptomyces coelicolor</named-content> and the Dormancy Regulator DevR of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content> Control Overlapping Regulons
title_full_unstemmed	OsdR of <named-content content-type="genus-species">Streptomyces coelicolor</named-content> and the Dormancy Regulator DevR of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content> Control Overlapping Regulons
title_sort	osdr of <named-content content-type="genus-species">streptomyces coelicolor</named-content> and the dormancy regulator devr of <named-content content-type="genus-species">mycobacterium tuberculosis</named-content> control overlapping regulons
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/d0d85a81b67a4222a27d115c79c8e771
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OsdR of <named-content content-type="genus-species">Streptomyces coelicolor</named-content> and the Dormancy Regulator DevR of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content> Control Overlapping Regulons

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