Abstract

ABSTRACTPresent 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.

Highlights

  • Present in every kingdom of life, generally in multiple copies, DEAD-box RNA helicases are specialized enzymes that unwind RNA secondary structures

  • We previously discovered the existence of a minimal RNA degradosome in H. pylori composed of the essential RNase J ribonuclease and of a newly identified DEAD-box RNA helicase that we designated RhpA [4]

  • The tree obtained with RNase J suggests that the rnj genes were vertically transmitted from the last common ancestor of Epsilonproteobacteria species

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Summary

Introduction

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. RhpA regulates transcription of the rnj gene encoding RNase J, its essential partner in the minimal H. pylori RNA degradosome, and plays a crucial role in the control of RNA decay. As a core component of RNA degradosomes, DEAD-box helicases have a global role in the control of RNA processing and mRNA turnover in several bacterial species, including E. coli, S. aureus, B. subtilis, and H. pylori [1, 4, 19, 20]

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