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Functional expansion of a TCA cycle operon mRNA by a 3′ end-derived small RNA

Global RNA profiling studies in bacteria have predicted the existence of many of small noncoding RNAs (sRNAs) that are processed off mRNA 3′ ends to regulate other mRNAs via the RNA chaperones Hfq and ProQ. Here, we present targets of SdhX (RybD), an Hfq-dependent sRNA that is generated by RNase E m...

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Autores principales: Miyakoshi, Masatoshi, Matera, Gianluca, Maki, Kanako, Sone, Yasuhiro, Vogel, Jörg
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6393394/
https://www.ncbi.nlm.nih.gov/pubmed/30541135
http://dx.doi.org/10.1093/nar/gky1243
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author Miyakoshi, Masatoshi
Matera, Gianluca
Maki, Kanako
Sone, Yasuhiro
Vogel, Jörg
author_facet Miyakoshi, Masatoshi
Matera, Gianluca
Maki, Kanako
Sone, Yasuhiro
Vogel, Jörg
author_sort Miyakoshi, Masatoshi
collection PubMed
description Global RNA profiling studies in bacteria have predicted the existence of many of small noncoding RNAs (sRNAs) that are processed off mRNA 3′ ends to regulate other mRNAs via the RNA chaperones Hfq and ProQ. Here, we present targets of SdhX (RybD), an Hfq-dependent sRNA that is generated by RNase E mediated 3′ processing of the ∼10 000-nt mRNA of the TCA cycle operon sdhCDAB-sucABCD in enteric bacteria. An in silico search predicted ackA mRNA, which encodes acetate kinase, as a conserved primary target of SdhX. Through base pairing, SdhX represses AckA synthesis during growth of Salmonella on acetate. Repression can be achieved by a naturally occurring 38-nucleotide SdhX variant, revealing the shortest functional Hfq-associated sRNA yet. Salmonella SdhX also targets the mRNAs of fumB (anaerobic fumarase) and yfbV, a gene of unknown function adjacent to ackA. Instead, through a slightly different seed sequence, SdhX can repress other targets in Escherichia coli, namely katG (catalase) and fdoG (aerobic formate dehydrogenase). This study illustrates how a key operon from central metabolism is functionally connected to other metabolic pathways through a 3′ appended sRNA, and supports the notion that mRNA 3′UTRs are a playground for the evolution of regulatory RNA networks in bacteria.
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spelling pubmed-63933942019-03-05 Functional expansion of a TCA cycle operon mRNA by a 3′ end-derived small RNA Miyakoshi, Masatoshi Matera, Gianluca Maki, Kanako Sone, Yasuhiro Vogel, Jörg Nucleic Acids Res RNA and RNA-protein complexes Global RNA profiling studies in bacteria have predicted the existence of many of small noncoding RNAs (sRNAs) that are processed off mRNA 3′ ends to regulate other mRNAs via the RNA chaperones Hfq and ProQ. Here, we present targets of SdhX (RybD), an Hfq-dependent sRNA that is generated by RNase E mediated 3′ processing of the ∼10 000-nt mRNA of the TCA cycle operon sdhCDAB-sucABCD in enteric bacteria. An in silico search predicted ackA mRNA, which encodes acetate kinase, as a conserved primary target of SdhX. Through base pairing, SdhX represses AckA synthesis during growth of Salmonella on acetate. Repression can be achieved by a naturally occurring 38-nucleotide SdhX variant, revealing the shortest functional Hfq-associated sRNA yet. Salmonella SdhX also targets the mRNAs of fumB (anaerobic fumarase) and yfbV, a gene of unknown function adjacent to ackA. Instead, through a slightly different seed sequence, SdhX can repress other targets in Escherichia coli, namely katG (catalase) and fdoG (aerobic formate dehydrogenase). This study illustrates how a key operon from central metabolism is functionally connected to other metabolic pathways through a 3′ appended sRNA, and supports the notion that mRNA 3′UTRs are a playground for the evolution of regulatory RNA networks in bacteria. Oxford University Press 2019-02-28 2018-12-12 /pmc/articles/PMC6393394/ /pubmed/30541135 http://dx.doi.org/10.1093/nar/gky1243 Text en © The Author(s) 2018. Published by Oxford University Press on behalf of Nucleic Acids Research. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle RNA and RNA-protein complexes
Miyakoshi, Masatoshi
Matera, Gianluca
Maki, Kanako
Sone, Yasuhiro
Vogel, Jörg
Functional expansion of a TCA cycle operon mRNA by a 3′ end-derived small RNA
title Functional expansion of a TCA cycle operon mRNA by a 3′ end-derived small RNA
title_full Functional expansion of a TCA cycle operon mRNA by a 3′ end-derived small RNA
title_fullStr Functional expansion of a TCA cycle operon mRNA by a 3′ end-derived small RNA
title_full_unstemmed Functional expansion of a TCA cycle operon mRNA by a 3′ end-derived small RNA
title_short Functional expansion of a TCA cycle operon mRNA by a 3′ end-derived small RNA
title_sort functional expansion of a tca cycle operon mrna by a 3′ end-derived small rna
topic RNA and RNA-protein complexes
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6393394/
https://www.ncbi.nlm.nih.gov/pubmed/30541135
http://dx.doi.org/10.1093/nar/gky1243
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