Hfq and RNase R Mediate rRNA Processing and Degradation in a Novel RNA Quality Control Process

ABSTRACT RNA quality control pathways are critical for cell survival. Here, we describe a new surveillance process involved in the degradation of highly structured and stable ribosomal RNAs. The results demonstrated that the RNA chaperone Hfq and the 3′–5′ exoribonuclease R mediate the elimination o...

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Autores principales:	Ricardo F. dos Santos, José M. Andrade, Joana Pissarra, Murray P. Deutscher, Cecília M. Arraiano
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Hfq RNA maturation RNA processing RNA quality control RNase R ribosomal RNA Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c6bb3b6f9e5e472f890bdfa84568ada4
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spelling	oai:doaj.org-article:c6bb3b6f9e5e472f890bdfa84568ada42021-11-15T16:19:08ZHfq and RNase R Mediate rRNA Processing and Degradation in a Novel RNA Quality Control Process10.1128/mBio.02398-202150-7511https://doaj.org/article/c6bb3b6f9e5e472f890bdfa84568ada42020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02398-20https://doaj.org/toc/2150-7511ABSTRACT RNA quality control pathways are critical for cell survival. Here, we describe a new surveillance process involved in the degradation of highly structured and stable ribosomal RNAs. The results demonstrated that the RNA chaperone Hfq and the 3′–5′ exoribonuclease R mediate the elimination of detrimental rRNA fragments and are required for the correct processing of rRNA precursors. Escherichia coli cells lacking both Hfq and RNase R accumulate a high level of 16S- and 23S-derived rRNA fragments. Hfq and RNase R were also shown to participate in the maturation of 16S and 23S rRNA precursors. This correlates with the fact that in the absence of Hfq and RNase R, there are severe ribosome assembly defects and a sharp reduction in 70S ribosome levels. Hfq and RNase R may act independently or in a complex, as protein interaction studies revealed that these RNA-binding proteins can associate. This is the first demonstration that the well-conserved Hfq and RNase R proteins act on common regulatory pathways, unraveling previously unknown mechanisms of rRNA surveillance with important consequences for translation and cell survival. IMPORTANCE Quality control pathways that oversee the quality of stable RNA molecules are critical for the cell. In this work, we demonstrate, for the first time, a functional link between Hfq and RNase R in the processing and degradation of the highly structured rRNAs. These RNA-binding proteins are required for the maturation of 16S and 23S rRNAs and correct ribosome assembly. Furthermore, they participate in the degradation of rRNAs and clearance of toxic rRNA fragments from the cell. Our studies have also shown that Hfq and RNase R can form a complex. In summary, the cooperation between Hfq and RNase R in metabolic pathways of stable RNAs may represent a broader mechanism of RNA quality control, given the high conservation of these RNA-binding proteins throughout evolution.Ricardo F. dos SantosJosé M. AndradeJoana PissarraMurray P. DeutscherCecília M. ArraianoAmerican Society for MicrobiologyarticleHfqRNA maturationRNA processingRNA quality controlRNase Rribosomal RNAMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Hfq RNA maturation RNA processing RNA quality control RNase R ribosomal RNA Microbiology QR1-502
spellingShingle	Hfq RNA maturation RNA processing RNA quality control RNase R ribosomal RNA Microbiology QR1-502 Ricardo F. dos Santos José M. Andrade Joana Pissarra Murray P. Deutscher Cecília M. Arraiano Hfq and RNase R Mediate rRNA Processing and Degradation in a Novel RNA Quality Control Process
description	ABSTRACT RNA quality control pathways are critical for cell survival. Here, we describe a new surveillance process involved in the degradation of highly structured and stable ribosomal RNAs. The results demonstrated that the RNA chaperone Hfq and the 3′–5′ exoribonuclease R mediate the elimination of detrimental rRNA fragments and are required for the correct processing of rRNA precursors. Escherichia coli cells lacking both Hfq and RNase R accumulate a high level of 16S- and 23S-derived rRNA fragments. Hfq and RNase R were also shown to participate in the maturation of 16S and 23S rRNA precursors. This correlates with the fact that in the absence of Hfq and RNase R, there are severe ribosome assembly defects and a sharp reduction in 70S ribosome levels. Hfq and RNase R may act independently or in a complex, as protein interaction studies revealed that these RNA-binding proteins can associate. This is the first demonstration that the well-conserved Hfq and RNase R proteins act on common regulatory pathways, unraveling previously unknown mechanisms of rRNA surveillance with important consequences for translation and cell survival. IMPORTANCE Quality control pathways that oversee the quality of stable RNA molecules are critical for the cell. In this work, we demonstrate, for the first time, a functional link between Hfq and RNase R in the processing and degradation of the highly structured rRNAs. These RNA-binding proteins are required for the maturation of 16S and 23S rRNAs and correct ribosome assembly. Furthermore, they participate in the degradation of rRNAs and clearance of toxic rRNA fragments from the cell. Our studies have also shown that Hfq and RNase R can form a complex. In summary, the cooperation between Hfq and RNase R in metabolic pathways of stable RNAs may represent a broader mechanism of RNA quality control, given the high conservation of these RNA-binding proteins throughout evolution.
format	article
author	Ricardo F. dos Santos José M. Andrade Joana Pissarra Murray P. Deutscher Cecília M. Arraiano
author_facet	Ricardo F. dos Santos José M. Andrade Joana Pissarra Murray P. Deutscher Cecília M. Arraiano
author_sort	Ricardo F. dos Santos
title	Hfq and RNase R Mediate rRNA Processing and Degradation in a Novel RNA Quality Control Process
title_short	Hfq and RNase R Mediate rRNA Processing and Degradation in a Novel RNA Quality Control Process
title_full	Hfq and RNase R Mediate rRNA Processing and Degradation in a Novel RNA Quality Control Process
title_fullStr	Hfq and RNase R Mediate rRNA Processing and Degradation in a Novel RNA Quality Control Process
title_full_unstemmed	Hfq and RNase R Mediate rRNA Processing and Degradation in a Novel RNA Quality Control Process
title_sort	hfq and rnase r mediate rrna processing and degradation in a novel rna quality control process
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/c6bb3b6f9e5e472f890bdfa84568ada4
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Hfq and RNase R Mediate rRNA Processing and Degradation in a Novel RNA Quality Control Process

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