Sigma 54-Regulated Transcription Is Associated with Membrane Reorganization and Type III Secretion Effectors during Conversion to Infectious Forms of <named-content content-type="genus-species">Chlamydia trachomatis</named-content>

ABSTRACT Chlamydia bacteria are obligate intracellular organisms with a phylum-defining biphasic developmental cycle that is intrinsically linked to its ability to cause disease. The progression of the chlamydial developmental cycle is regulated by the temporal expression of genes predominantly cont...

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Autores principales:	Katelyn R. Soules, Scott D. LaBrie, Benjamin H. May, P. Scott Hefty
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Chlamydia trachomatis gene regulation regulon sigma factors Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/9251d9ea4e5a4129996c5154b1f0210c
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spelling	oai:doaj.org-article:9251d9ea4e5a4129996c5154b1f0210c2021-11-15T16:19:08ZSigma 54-Regulated Transcription Is Associated with Membrane Reorganization and Type III Secretion Effectors during Conversion to Infectious Forms of <named-content content-type="genus-species">Chlamydia trachomatis</named-content>10.1128/mBio.01725-202150-7511https://doaj.org/article/9251d9ea4e5a4129996c5154b1f0210c2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01725-20https://doaj.org/toc/2150-7511ABSTRACT Chlamydia bacteria are obligate intracellular organisms with a phylum-defining biphasic developmental cycle that is intrinsically linked to its ability to cause disease. The progression of the chlamydial developmental cycle is regulated by the temporal expression of genes predominantly controlled by RNA polymerase sigma (σ) factors. Sigma 54 (σ54) is one of three sigma factors encoded by Chlamydia for which the role and regulon are unknown. CtcC is part of a two-component signal transduction system that is requisite for σ54 transcriptional activation. CtcC activation of σ54 requires phosphorylation, which relieves inhibition by the CtcC regulatory domain and enables ATP hydrolysis by the ATPase domain. Prior studies with CtcC homologs in other organisms have shown that expression of the ATPase domain alone can activate σ54 transcription. Biochemical analysis of CtcC ATPase domain supported the idea of ATP hydrolysis occurring in the absence of the regulatory domain, as well as the presence of an active-site residue essential for ATPase activity (E242). Using recently developed genetic approaches in Chlamydia to induce expression of the CtcC ATPase domain, a transcriptional profile was determined that is expected to reflect the σ54 regulon. Computational evaluation revealed that the majority of the differentially expressed genes were preceded by highly conserved σ54 promoter elements. Reporter gene analyses using these putative σ54 promoters reinforced the accuracy of the model of the proposed regulon. Investigation of the gene products included in this regulon supports the idea that σ54 controls expression of genes that are critical for conversion of Chlamydia from replicative reticulate bodies into infectious elementary bodies. IMPORTANCE The factors that control the growth and infectious processes for Chlamydia are still poorly understood. This study used recently developed genetic tools to determine the regulon for one of the key transcription factors encoded by Chlamydia, sigma 54. Surrogate and computational analyses provide additional support for the hypothesis that sigma 54 plays a key role in controlling the expression of many components critical to converting and enabling the infectious capability of Chlamydia. These components include those that remodel the membrane for the extracellular environment and incorporation of an arsenal of type III secretion effectors in preparation for infecting new cells.Katelyn R. SoulesScott D. LaBrieBenjamin H. MayP. Scott HeftyAmerican Society for MicrobiologyarticleChlamydia trachomatisgene regulationregulonsigma factorsMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Chlamydia trachomatis gene regulation regulon sigma factors Microbiology QR1-502
spellingShingle	Chlamydia trachomatis gene regulation regulon sigma factors Microbiology QR1-502 Katelyn R. Soules Scott D. LaBrie Benjamin H. May P. Scott Hefty Sigma 54-Regulated Transcription Is Associated with Membrane Reorganization and Type III Secretion Effectors during Conversion to Infectious Forms of <named-content content-type="genus-species">Chlamydia trachomatis</named-content>
description	ABSTRACT Chlamydia bacteria are obligate intracellular organisms with a phylum-defining biphasic developmental cycle that is intrinsically linked to its ability to cause disease. The progression of the chlamydial developmental cycle is regulated by the temporal expression of genes predominantly controlled by RNA polymerase sigma (σ) factors. Sigma 54 (σ54) is one of three sigma factors encoded by Chlamydia for which the role and regulon are unknown. CtcC is part of a two-component signal transduction system that is requisite for σ54 transcriptional activation. CtcC activation of σ54 requires phosphorylation, which relieves inhibition by the CtcC regulatory domain and enables ATP hydrolysis by the ATPase domain. Prior studies with CtcC homologs in other organisms have shown that expression of the ATPase domain alone can activate σ54 transcription. Biochemical analysis of CtcC ATPase domain supported the idea of ATP hydrolysis occurring in the absence of the regulatory domain, as well as the presence of an active-site residue essential for ATPase activity (E242). Using recently developed genetic approaches in Chlamydia to induce expression of the CtcC ATPase domain, a transcriptional profile was determined that is expected to reflect the σ54 regulon. Computational evaluation revealed that the majority of the differentially expressed genes were preceded by highly conserved σ54 promoter elements. Reporter gene analyses using these putative σ54 promoters reinforced the accuracy of the model of the proposed regulon. Investigation of the gene products included in this regulon supports the idea that σ54 controls expression of genes that are critical for conversion of Chlamydia from replicative reticulate bodies into infectious elementary bodies. IMPORTANCE The factors that control the growth and infectious processes for Chlamydia are still poorly understood. This study used recently developed genetic tools to determine the regulon for one of the key transcription factors encoded by Chlamydia, sigma 54. Surrogate and computational analyses provide additional support for the hypothesis that sigma 54 plays a key role in controlling the expression of many components critical to converting and enabling the infectious capability of Chlamydia. These components include those that remodel the membrane for the extracellular environment and incorporation of an arsenal of type III secretion effectors in preparation for infecting new cells.
format	article
author	Katelyn R. Soules Scott D. LaBrie Benjamin H. May P. Scott Hefty
author_facet	Katelyn R. Soules Scott D. LaBrie Benjamin H. May P. Scott Hefty
author_sort	Katelyn R. Soules
title	Sigma 54-Regulated Transcription Is Associated with Membrane Reorganization and Type III Secretion Effectors during Conversion to Infectious Forms of <named-content content-type="genus-species">Chlamydia trachomatis</named-content>
title_short	Sigma 54-Regulated Transcription Is Associated with Membrane Reorganization and Type III Secretion Effectors during Conversion to Infectious Forms of <named-content content-type="genus-species">Chlamydia trachomatis</named-content>
title_full	Sigma 54-Regulated Transcription Is Associated with Membrane Reorganization and Type III Secretion Effectors during Conversion to Infectious Forms of <named-content content-type="genus-species">Chlamydia trachomatis</named-content>
title_fullStr	Sigma 54-Regulated Transcription Is Associated with Membrane Reorganization and Type III Secretion Effectors during Conversion to Infectious Forms of <named-content content-type="genus-species">Chlamydia trachomatis</named-content>
title_full_unstemmed	Sigma 54-Regulated Transcription Is Associated with Membrane Reorganization and Type III Secretion Effectors during Conversion to Infectious Forms of <named-content content-type="genus-species">Chlamydia trachomatis</named-content>
title_sort	sigma 54-regulated transcription is associated with membrane reorganization and type iii secretion effectors during conversion to infectious forms of <named-content content-type="genus-species">chlamydia trachomatis</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/9251d9ea4e5a4129996c5154b1f0210c
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Sigma 54-Regulated Transcription Is Associated with Membrane Reorganization and Type III Secretion Effectors during Conversion to Infectious Forms of <named-content content-type="genus-species">Chlamydia trachomatis</named-content>

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