BldC Delays Entry into Development To Produce a Sustained Period of Vegetative Growth in <named-content content-type="genus-species">Streptomyces venezuelae</named-content>

ABSTRACT Streptomycetes are filamentous bacteria that differentiate by producing spore-bearing reproductive structures called aerial hyphae. The transition from vegetative to reproductive growth is controlled by the bld (bald) loci, and mutations in bld genes prevent the formation of aerial hyphae,...

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Autores principales:	Matthew J. Bush, Govind Chandra, Mahmoud M. Al-Bassam, Kim C. Findlay, Mark J. Buttner
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	cell division morphological differentiation sporulation transcriptional regulation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/05f97b4d71b94da8a4c2b62aad548af3
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spelling	oai:doaj.org-article:05f97b4d71b94da8a4c2b62aad548af32021-11-15T15:55:14ZBldC Delays Entry into Development To Produce a Sustained Period of Vegetative Growth in <named-content content-type="genus-species">Streptomyces venezuelae</named-content>10.1128/mBio.02812-182150-7511https://doaj.org/article/05f97b4d71b94da8a4c2b62aad548af32019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02812-18https://doaj.org/toc/2150-7511ABSTRACT Streptomycetes are filamentous bacteria that differentiate by producing spore-bearing reproductive structures called aerial hyphae. The transition from vegetative to reproductive growth is controlled by the bld (bald) loci, and mutations in bld genes prevent the formation of aerial hyphae, either by blocking entry into development (typically mutations in activators) or by inducing precocious sporulation in the vegetative mycelium (typically mutations in repressors). One of the bld genes, bldC, encodes a 68-residue DNA-binding protein related to the DNA-binding domain of MerR-family transcription factors. Recent work has shown that BldC binds DNA by a novel mechanism, but there is less insight into its impact on Streptomyces development. Here we used ChIP-seq coupled with RNA-seq to define the BldC regulon in the model species Streptomyces venezuelae, showing that BldC can function both as a repressor and as an activator of transcription. Using electron microscopy and time-lapse imaging, we show that bldC mutants are bald because they initiate development prematurely, bypassing the formation of aerial hyphae. This is consistent with the premature expression of BldC target genes encoding proteins with key roles in development (e.g., whiD, whiI, sigF), chromosome condensation and segregation (e.g., smeA-sffA, hupS), and sporulation-specific cell division (e.g., dynAB), suggesting that BldC-mediated repression is critical to maintain a sustained period of vegetative growth prior to sporulation. We discuss the possible significance of BldC as an evolutionary link between MerR family transcription factors and DNA architectural proteins. IMPORTANCE Understanding the mechanisms that drive bacterial morphogenesis depends on the dissection of the regulatory networks that underpin the cell biological processes involved. Recently, Streptomyces venezuelae has emerged as an attractive model system for the study of morphological differentiation in Streptomyces. This has led to significant progress in identifying the genes controlled by the transcription factors that regulate aerial mycelium formation (Bld regulators) and sporulation (Whi regulators). Taking advantage of S. venezuelae, we used ChIP-seq coupled with RNA-seq to identify the genes directly under the control of BldC. Because S. venezuelae sporulates in liquid culture, the complete spore-to-spore life cycle can be examined using time-lapse microscopy, and we applied this technique to the bldC mutant. These combined approaches reveal BldC to be a member of an emerging class of Bld regulators that function principally to repress key sporulation genes, thereby extending vegetative growth and blocking the onset of morphological differentiation.Matthew J. BushGovind ChandraMahmoud M. Al-BassamKim C. FindlayMark J. ButtnerAmerican Society for Microbiologyarticlecell divisionmorphological differentiationsporulationtranscriptional regulationMicrobiologyQR1-502ENmBio, Vol 10, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	cell division morphological differentiation sporulation transcriptional regulation Microbiology QR1-502
spellingShingle	cell division morphological differentiation sporulation transcriptional regulation Microbiology QR1-502 Matthew J. Bush Govind Chandra Mahmoud M. Al-Bassam Kim C. Findlay Mark J. Buttner BldC Delays Entry into Development To Produce a Sustained Period of Vegetative Growth in <named-content content-type="genus-species">Streptomyces venezuelae</named-content>
description	ABSTRACT Streptomycetes are filamentous bacteria that differentiate by producing spore-bearing reproductive structures called aerial hyphae. The transition from vegetative to reproductive growth is controlled by the bld (bald) loci, and mutations in bld genes prevent the formation of aerial hyphae, either by blocking entry into development (typically mutations in activators) or by inducing precocious sporulation in the vegetative mycelium (typically mutations in repressors). One of the bld genes, bldC, encodes a 68-residue DNA-binding protein related to the DNA-binding domain of MerR-family transcription factors. Recent work has shown that BldC binds DNA by a novel mechanism, but there is less insight into its impact on Streptomyces development. Here we used ChIP-seq coupled with RNA-seq to define the BldC regulon in the model species Streptomyces venezuelae, showing that BldC can function both as a repressor and as an activator of transcription. Using electron microscopy and time-lapse imaging, we show that bldC mutants are bald because they initiate development prematurely, bypassing the formation of aerial hyphae. This is consistent with the premature expression of BldC target genes encoding proteins with key roles in development (e.g., whiD, whiI, sigF), chromosome condensation and segregation (e.g., smeA-sffA, hupS), and sporulation-specific cell division (e.g., dynAB), suggesting that BldC-mediated repression is critical to maintain a sustained period of vegetative growth prior to sporulation. We discuss the possible significance of BldC as an evolutionary link between MerR family transcription factors and DNA architectural proteins. IMPORTANCE Understanding the mechanisms that drive bacterial morphogenesis depends on the dissection of the regulatory networks that underpin the cell biological processes involved. Recently, Streptomyces venezuelae has emerged as an attractive model system for the study of morphological differentiation in Streptomyces. This has led to significant progress in identifying the genes controlled by the transcription factors that regulate aerial mycelium formation (Bld regulators) and sporulation (Whi regulators). Taking advantage of S. venezuelae, we used ChIP-seq coupled with RNA-seq to identify the genes directly under the control of BldC. Because S. venezuelae sporulates in liquid culture, the complete spore-to-spore life cycle can be examined using time-lapse microscopy, and we applied this technique to the bldC mutant. These combined approaches reveal BldC to be a member of an emerging class of Bld regulators that function principally to repress key sporulation genes, thereby extending vegetative growth and blocking the onset of morphological differentiation.
format	article
author	Matthew J. Bush Govind Chandra Mahmoud M. Al-Bassam Kim C. Findlay Mark J. Buttner
author_facet	Matthew J. Bush Govind Chandra Mahmoud M. Al-Bassam Kim C. Findlay Mark J. Buttner
author_sort	Matthew J. Bush
title	BldC Delays Entry into Development To Produce a Sustained Period of Vegetative Growth in <named-content content-type="genus-species">Streptomyces venezuelae</named-content>
title_short	BldC Delays Entry into Development To Produce a Sustained Period of Vegetative Growth in <named-content content-type="genus-species">Streptomyces venezuelae</named-content>
title_full	BldC Delays Entry into Development To Produce a Sustained Period of Vegetative Growth in <named-content content-type="genus-species">Streptomyces venezuelae</named-content>
title_fullStr	BldC Delays Entry into Development To Produce a Sustained Period of Vegetative Growth in <named-content content-type="genus-species">Streptomyces venezuelae</named-content>
title_full_unstemmed	BldC Delays Entry into Development To Produce a Sustained Period of Vegetative Growth in <named-content content-type="genus-species">Streptomyces venezuelae</named-content>
title_sort	bldc delays entry into development to produce a sustained period of vegetative growth in <named-content content-type="genus-species">streptomyces venezuelae</named-content>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/05f97b4d71b94da8a4c2b62aad548af3
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BldC Delays Entry into Development To Produce a Sustained Period of Vegetative Growth in <named-content content-type="genus-species">Streptomyces venezuelae</named-content>

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