Bacterial Noncoding RNAs Excised from within Protein-Coding Transcripts

ABSTRACT Prokaryotic genomes encode a plethora of small noncoding RNAs (ncRNAs) that fine-tune the expression of specific genes. The vast majority of known bacterial ncRNAs are encoded from within intergenic regions, where their expression is controlled by promoter and terminator elements, similarly...

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Autores principales: Daniel Dar, Rotem Sorek
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:ab9dd11446ad46ffb3dffd7b4b73eede2021-11-15T15:58:21ZBacterial Noncoding RNAs Excised from within Protein-Coding Transcripts10.1128/mBio.01730-182150-7511https://doaj.org/article/ab9dd11446ad46ffb3dffd7b4b73eede2018-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01730-18https://doaj.org/toc/2150-7511ABSTRACT Prokaryotic genomes encode a plethora of small noncoding RNAs (ncRNAs) that fine-tune the expression of specific genes. The vast majority of known bacterial ncRNAs are encoded from within intergenic regions, where their expression is controlled by promoter and terminator elements, similarly to protein-coding genes. In addition, recent studies have shown that functional ncRNAs can also be derived from gene 3′ untranslated regions (3′UTRs) via an alternative biogenesis pathway, in which the ncRNA segment is separated from the mRNA via RNase cleavage. Here, we report the detection of a large set of decay-generated noncoding RNAs (decRNAs), many of which are completely embedded within protein-coding mRNA regions rather than in the UTRs. We show that these decRNAs are “carved out” of the mRNA through the action of RNase E and that they are predicted to fold into highly stable RNA structures, similar to those of known ncRNAs. A subset of these decRNAs is predicted to interact with Hfq or ProQ or both, which act as ncRNA chaperones, and some decRNAs display evolutionarily conserved sequences and conserved expression patterns between different species. These results suggest that mRNA protein-coding regions may harbor a large set of potentially functional small RNAs. IMPORTANCE Bacteria and archaea utilize regulatory small noncoding RNAs (ncRNAs) to control the expression of specific genetic programs. These ncRNAs are almost exclusively encoded within intergenic regions and are independently transcribed. Here, we report on a large set ncRNAs that are “carved out” from within the protein-coding regions of Escherichia coli mRNAs by cellular RNases. These protected mRNA fragments fold into energetically stable RNA structures, reminiscent of those of intergenic regulatory ncRNAs. In addition, a subset of these ncRNAs coprecipitate with the major ncRNA chaperones Hfq and ProQ and display evolutionarily conserved sequences and conserved expression patterns between different bacterial species. Our data suggest that protein-coding genes can potentially act as a reservoir of regulatory ncRNAs.Daniel DarRotem SorekAmerican Society for MicrobiologyarticletranscriptomemRNA degradationncRNAsRNAMicrobiologyQR1-502ENmBio, Vol 9, Iss 5 (2018)
institution DOAJ
collection DOAJ
language EN
topic transcriptome
mRNA degradation
ncRNA
sRNA
Microbiology
QR1-502
spellingShingle transcriptome
mRNA degradation
ncRNA
sRNA
Microbiology
QR1-502
Daniel Dar
Rotem Sorek
Bacterial Noncoding RNAs Excised from within Protein-Coding Transcripts
description ABSTRACT Prokaryotic genomes encode a plethora of small noncoding RNAs (ncRNAs) that fine-tune the expression of specific genes. The vast majority of known bacterial ncRNAs are encoded from within intergenic regions, where their expression is controlled by promoter and terminator elements, similarly to protein-coding genes. In addition, recent studies have shown that functional ncRNAs can also be derived from gene 3′ untranslated regions (3′UTRs) via an alternative biogenesis pathway, in which the ncRNA segment is separated from the mRNA via RNase cleavage. Here, we report the detection of a large set of decay-generated noncoding RNAs (decRNAs), many of which are completely embedded within protein-coding mRNA regions rather than in the UTRs. We show that these decRNAs are “carved out” of the mRNA through the action of RNase E and that they are predicted to fold into highly stable RNA structures, similar to those of known ncRNAs. A subset of these decRNAs is predicted to interact with Hfq or ProQ or both, which act as ncRNA chaperones, and some decRNAs display evolutionarily conserved sequences and conserved expression patterns between different species. These results suggest that mRNA protein-coding regions may harbor a large set of potentially functional small RNAs. IMPORTANCE Bacteria and archaea utilize regulatory small noncoding RNAs (ncRNAs) to control the expression of specific genetic programs. These ncRNAs are almost exclusively encoded within intergenic regions and are independently transcribed. Here, we report on a large set ncRNAs that are “carved out” from within the protein-coding regions of Escherichia coli mRNAs by cellular RNases. These protected mRNA fragments fold into energetically stable RNA structures, reminiscent of those of intergenic regulatory ncRNAs. In addition, a subset of these ncRNAs coprecipitate with the major ncRNA chaperones Hfq and ProQ and display evolutionarily conserved sequences and conserved expression patterns between different bacterial species. Our data suggest that protein-coding genes can potentially act as a reservoir of regulatory ncRNAs.
format article
author Daniel Dar
Rotem Sorek
author_facet Daniel Dar
Rotem Sorek
author_sort Daniel Dar
title Bacterial Noncoding RNAs Excised from within Protein-Coding Transcripts
title_short Bacterial Noncoding RNAs Excised from within Protein-Coding Transcripts
title_full Bacterial Noncoding RNAs Excised from within Protein-Coding Transcripts
title_fullStr Bacterial Noncoding RNAs Excised from within Protein-Coding Transcripts
title_full_unstemmed Bacterial Noncoding RNAs Excised from within Protein-Coding Transcripts
title_sort bacterial noncoding rnas excised from within protein-coding transcripts
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/ab9dd11446ad46ffb3dffd7b4b73eede
work_keys_str_mv AT danieldar bacterialnoncodingrnasexcisedfromwithinproteincodingtranscripts
AT rotemsorek bacterialnoncodingrnasexcisedfromwithinproteincodingtranscripts
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