The Sole DEAD-Box RNA Helicase of the Gastric Pathogen <italic toggle="yes">Helicobacter pylori</italic> Is Essential for Colonization

ABSTRACT Present in every kingdom of life, generally in multiple copies, DEAD-box RNA helicases are specialized enzymes that unwind RNA secondary structures. They play major roles in mRNA decay, ribosome biogenesis, and adaptation to cold temperatures. Most bacteria have multiple DEAD-box helicases...

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Autores principales:	Lamya El Mortaji, Sylvie Aubert, Eloïse Galtier, Christine Schmitt, Karine Anger, Yulia Redko, Yves Quentin, Hilde De Reuse
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	DEAD-box helicase Helicobacter pylori RNA degradation flagellar motility mouse model Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8f920e10452e4a789f24d69a88c8fb40
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spelling	oai:doaj.org-article:8f920e10452e4a789f24d69a88c8fb402021-11-15T15:53:27ZThe Sole DEAD-Box RNA Helicase of the Gastric Pathogen <italic toggle="yes">Helicobacter pylori</italic> Is Essential for Colonization10.1128/mBio.02071-172150-7511https://doaj.org/article/8f920e10452e4a789f24d69a88c8fb402018-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02071-17https://doaj.org/toc/2150-7511ABSTRACT Present in every kingdom of life, generally in multiple copies, DEAD-box RNA helicases are specialized enzymes that unwind RNA secondary structures. They play major roles in mRNA decay, ribosome biogenesis, and adaptation to cold temperatures. Most bacteria have multiple DEAD-box helicases that present both specialized and partially redundant functions. By using phylogenomics, we revealed that the Helicobacter genus, including the major gastric pathogen H. pylori, is among the exceptions, as it encodes a sole DEAD-box RNA helicase. In H. pylori, this helicase, designated RhpA, forms a minimal RNA degradosome together with the essential RNase, RNase J, a major player in the control of RNA decay. Here, we used H. pylori as a model organism with a sole DEAD-box helicase and investigated the role of this helicase in H. pylori physiology, ribosome assembly, and during in vivo colonization. Our data showed that RhpA is dispensable for growth at 37°C but crucial at 33°C, suggesting an essential role of the helicase in cold adaptation. Moreover, we found that a ΔrhpA mutant was impaired in motility and deficient in colonization of the mouse model. RhpA is involved in the maturation of 16S rRNA at 37°C and is associated with translating ribosomes. At 33°C, RhpA is, in addition, recruited to individual ribosomal subunits. Finally, via its role in the RNA degradosome, RhpA directs the regulation of the expression of its partner, RNase J. RhpA is thus a multifunctional enzyme that, in H. pylori, plays a central role in gene regulation and in the control of virulence. IMPORTANCE We present the results of our study on the role of RhpA, the sole DEAD-box RNA helicase encoded by the major gastric pathogen Helicobacter pylori. We observed that all the Helicobacter species possess such a sole helicase, in contrast to most free-living bacteria. RhpA is not essential for growth of H. pylori under normal conditions. However, deletion of rhpA leads to a motility defect and to total inhibition of the ability of H. pylori to colonize a mouse model. We also demonstrated that this helicase encompasses most of the functions of its specialized orthologs described so far. We found that RhpA is a key element of the bacterial adaptation to colder temperatures and plays a minor role in ribosome biogenesis. Finally, RhpA regulates transcription of the rnj gene encoding RNase J, its essential partner in the minimal H. pylori RNA degradosome, and thus plays a crucial role in the control of RNA decay.Lamya El MortajiSylvie AubertEloïse GaltierChristine SchmittKarine AngerYulia RedkoYves QuentinHilde De ReuseAmerican Society for MicrobiologyarticleDEAD-box helicaseHelicobacter pyloriRNA degradationflagellar motilitymouse modelMicrobiologyQR1-502ENmBio, Vol 9, Iss 2 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	DEAD-box helicase Helicobacter pylori RNA degradation flagellar motility mouse model Microbiology QR1-502
spellingShingle	DEAD-box helicase Helicobacter pylori RNA degradation flagellar motility mouse model Microbiology QR1-502 Lamya El Mortaji Sylvie Aubert Eloïse Galtier Christine Schmitt Karine Anger Yulia Redko Yves Quentin Hilde De Reuse The Sole DEAD-Box RNA Helicase of the Gastric Pathogen <italic toggle="yes">Helicobacter pylori</italic> Is Essential for Colonization
description	ABSTRACT Present in every kingdom of life, generally in multiple copies, DEAD-box RNA helicases are specialized enzymes that unwind RNA secondary structures. They play major roles in mRNA decay, ribosome biogenesis, and adaptation to cold temperatures. Most bacteria have multiple DEAD-box helicases that present both specialized and partially redundant functions. By using phylogenomics, we revealed that the Helicobacter genus, including the major gastric pathogen H. pylori, is among the exceptions, as it encodes a sole DEAD-box RNA helicase. In H. pylori, this helicase, designated RhpA, forms a minimal RNA degradosome together with the essential RNase, RNase J, a major player in the control of RNA decay. Here, we used H. pylori as a model organism with a sole DEAD-box helicase and investigated the role of this helicase in H. pylori physiology, ribosome assembly, and during in vivo colonization. Our data showed that RhpA is dispensable for growth at 37°C but crucial at 33°C, suggesting an essential role of the helicase in cold adaptation. Moreover, we found that a ΔrhpA mutant was impaired in motility and deficient in colonization of the mouse model. RhpA is involved in the maturation of 16S rRNA at 37°C and is associated with translating ribosomes. At 33°C, RhpA is, in addition, recruited to individual ribosomal subunits. Finally, via its role in the RNA degradosome, RhpA directs the regulation of the expression of its partner, RNase J. RhpA is thus a multifunctional enzyme that, in H. pylori, plays a central role in gene regulation and in the control of virulence. IMPORTANCE We present the results of our study on the role of RhpA, the sole DEAD-box RNA helicase encoded by the major gastric pathogen Helicobacter pylori. We observed that all the Helicobacter species possess such a sole helicase, in contrast to most free-living bacteria. RhpA is not essential for growth of H. pylori under normal conditions. However, deletion of rhpA leads to a motility defect and to total inhibition of the ability of H. pylori to colonize a mouse model. We also demonstrated that this helicase encompasses most of the functions of its specialized orthologs described so far. We found that RhpA is a key element of the bacterial adaptation to colder temperatures and plays a minor role in ribosome biogenesis. Finally, RhpA regulates transcription of the rnj gene encoding RNase J, its essential partner in the minimal H. pylori RNA degradosome, and thus plays a crucial role in the control of RNA decay.
format	article
author	Lamya El Mortaji Sylvie Aubert Eloïse Galtier Christine Schmitt Karine Anger Yulia Redko Yves Quentin Hilde De Reuse
author_facet	Lamya El Mortaji Sylvie Aubert Eloïse Galtier Christine Schmitt Karine Anger Yulia Redko Yves Quentin Hilde De Reuse
author_sort	Lamya El Mortaji
title	The Sole DEAD-Box RNA Helicase of the Gastric Pathogen <italic toggle="yes">Helicobacter pylori</italic> Is Essential for Colonization
title_short	The Sole DEAD-Box RNA Helicase of the Gastric Pathogen <italic toggle="yes">Helicobacter pylori</italic> Is Essential for Colonization
title_full	The Sole DEAD-Box RNA Helicase of the Gastric Pathogen <italic toggle="yes">Helicobacter pylori</italic> Is Essential for Colonization
title_fullStr	The Sole DEAD-Box RNA Helicase of the Gastric Pathogen <italic toggle="yes">Helicobacter pylori</italic> Is Essential for Colonization
title_full_unstemmed	The Sole DEAD-Box RNA Helicase of the Gastric Pathogen <italic toggle="yes">Helicobacter pylori</italic> Is Essential for Colonization
title_sort	sole dead-box rna helicase of the gastric pathogen <italic toggle="yes">helicobacter pylori</italic> is essential for colonization
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/8f920e10452e4a789f24d69a88c8fb40
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The Sole DEAD-Box RNA Helicase of the Gastric Pathogen <italic toggle="yes">Helicobacter pylori</italic> Is Essential for Colonization

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