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Maturation of atypical ribosomal RNA precursors in Helicobacter pylori

In most bacteria, ribosomal RNA is transcribed as a single polycistronic precursor that is first processed by RNase III. This double-stranded specific RNase cleaves two large stems flanking the 23S and 16S rRNA mature sequences, liberating three 16S, 23S and 5S rRNA precursors, which are further pro...

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Autores principales: Iost, Isabelle, Chabas, Sandrine, Darfeuille, Fabien
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6582327/
https://www.ncbi.nlm.nih.gov/pubmed/31006803
http://dx.doi.org/10.1093/nar/gkz258
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author Iost, Isabelle
Chabas, Sandrine
Darfeuille, Fabien
author_facet Iost, Isabelle
Chabas, Sandrine
Darfeuille, Fabien
author_sort Iost, Isabelle
collection PubMed
description In most bacteria, ribosomal RNA is transcribed as a single polycistronic precursor that is first processed by RNase III. This double-stranded specific RNase cleaves two large stems flanking the 23S and 16S rRNA mature sequences, liberating three 16S, 23S and 5S rRNA precursors, which are further processed by other ribonucleases. Here, we investigate the rRNA maturation pathway of the human gastric pathogen Helicobacter pylori. This bacterium has an unusual arrangement of its rRNA genes, the 16S rRNA gene being separated from a 23S-5S rRNA cluster. We show that RNase III also initiates processing in this organism, by cleaving two typical stem structures encompassing 16S and 23S rRNAs and an atypical stem–loop located upstream of the 5S rRNA. Deletion of RNase III leads to the accumulation of a large 23S-5S precursor that is found in polysomes, suggesting that it can function in translation. Finally, we characterize a cis-encoded antisense RNA overlapping the leader of the 23S-5S rRNA precursor. We present evidence that this antisense RNA interacts with this precursor, forming an intermolecular complex that is cleaved by RNase III. This pairing induces additional specific cleavages of the rRNA precursor coupled with a rapid degradation of the antisense RNA.
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spelling pubmed-65823272019-06-21 Maturation of atypical ribosomal RNA precursors in Helicobacter pylori Iost, Isabelle Chabas, Sandrine Darfeuille, Fabien Nucleic Acids Res RNA and RNA-protein complexes In most bacteria, ribosomal RNA is transcribed as a single polycistronic precursor that is first processed by RNase III. This double-stranded specific RNase cleaves two large stems flanking the 23S and 16S rRNA mature sequences, liberating three 16S, 23S and 5S rRNA precursors, which are further processed by other ribonucleases. Here, we investigate the rRNA maturation pathway of the human gastric pathogen Helicobacter pylori. This bacterium has an unusual arrangement of its rRNA genes, the 16S rRNA gene being separated from a 23S-5S rRNA cluster. We show that RNase III also initiates processing in this organism, by cleaving two typical stem structures encompassing 16S and 23S rRNAs and an atypical stem–loop located upstream of the 5S rRNA. Deletion of RNase III leads to the accumulation of a large 23S-5S precursor that is found in polysomes, suggesting that it can function in translation. Finally, we characterize a cis-encoded antisense RNA overlapping the leader of the 23S-5S rRNA precursor. We present evidence that this antisense RNA interacts with this precursor, forming an intermolecular complex that is cleaved by RNase III. This pairing induces additional specific cleavages of the rRNA precursor coupled with a rapid degradation of the antisense RNA. Oxford University Press 2019-06-20 2019-04-22 /pmc/articles/PMC6582327/ /pubmed/31006803 http://dx.doi.org/10.1093/nar/gkz258 Text en © The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle RNA and RNA-protein complexes
Iost, Isabelle
Chabas, Sandrine
Darfeuille, Fabien
Maturation of atypical ribosomal RNA precursors in Helicobacter pylori
title Maturation of atypical ribosomal RNA precursors in Helicobacter pylori
title_full Maturation of atypical ribosomal RNA precursors in Helicobacter pylori
title_fullStr Maturation of atypical ribosomal RNA precursors in Helicobacter pylori
title_full_unstemmed Maturation of atypical ribosomal RNA precursors in Helicobacter pylori
title_short Maturation of atypical ribosomal RNA precursors in Helicobacter pylori
title_sort maturation of atypical ribosomal rna precursors in helicobacter pylori
topic RNA and RNA-protein complexes
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6582327/
https://www.ncbi.nlm.nih.gov/pubmed/31006803
http://dx.doi.org/10.1093/nar/gkz258
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