The conserved 3' UTR-derived small RNA NarS mediates mRNA crossregulation during nitrate respiration
Small noncoding RNAs (sRNAs) from mRNA 3' UTRs seem to present a previously unrecognized layer of bacterial post-transcriptional control whereby mRNAs influence each other's expression, independently of transcriptional control. Studies in Escherichia coli and Salmonella enterica showed tha...
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Published in | Nucleic acids research Vol. 48; no. 4; pp. 2126 - 2143 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
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Oxford University Press
28.02.2020
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Abstract | Small noncoding RNAs (sRNAs) from mRNA 3' UTRs seem to present a previously unrecognized layer of bacterial post-transcriptional control whereby mRNAs influence each other's expression, independently of transcriptional control. Studies in Escherichia coli and Salmonella enterica showed that such sRNAs are natural products of RNase E-mediated mRNA decay and associate with major RNA-binding proteins (RBPs) such as Hfq and ProQ. If so, there must be additional sRNAs from mRNAs that accumulate only under specific physiological conditions. We test this prediction by characterizing candidate NarS that represents the 3' UTR of nitrate transporter NarK whose gene is silent during standard aerobic growth. We find that NarS acts by Hfq-dependent base pairing to repress the synthesis of the nitrite transporter, NirC, resulting in mRNA cross-regulation of nitrate and nitrite transporter genes. Interestingly, the NarS-mediated repression selectively targets the nirC cistron of the long nirBDC-cysG operon, an observation that we rationalize as a mechanism to protect the bacterial cytoplasm from excessive nitrite toxicity during anaerobic respiration with abundant nitrate. Our successful functional assignment of a 3' UTR sRNA from a non-standard growth condition supports the notion that mRNA crossregulation is more pervasive than currently appreciated. |
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AbstractList | Small noncoding RNAs (sRNAs) from mRNA 3′ UTRs seem to present a previously unrecognized layer of bacterial post-transcriptional control whereby mRNAs influence each other's expression, independently of transcriptional control. Studies in
Escherichia coli
and
Salmonella enterica
showed that such sRNAs are natural products of RNase E-mediated mRNA decay and associate with major RNA-binding proteins (RBPs) such as Hfq and ProQ. If so, there must be additional sRNAs from mRNAs that accumulate only under specific physiological conditions. We test this prediction by characterizing candidate NarS that represents the 3′ UTR of nitrate transporter NarK whose gene is silent during standard aerobic growth. We find that NarS acts by Hfq-dependent base pairing to repress the synthesis of the nitrite transporter, NirC, resulting in mRNA cross-regulation of nitrate and nitrite transporter genes. Interestingly, the NarS-mediated repression selectively targets the
nirC
cistron of the long
nirBDC
-
cysG
operon, an observation that we rationalize as a mechanism to protect the bacterial cytoplasm from excessive nitrite toxicity during anaerobic respiration with abundant nitrate. Our successful functional assignment of a 3′ UTR sRNA from a non-standard growth condition supports the notion that mRNA crossregulation is more pervasive than currently appreciated. Small noncoding RNAs (sRNAs) from mRNA 3' UTRs seem to present a previously unrecognized layer of bacterial post-transcriptional control whereby mRNAs influence each other's expression, independently of transcriptional control. Studies in Escherichia coli and Salmonella enterica showed that such sRNAs are natural products of RNase E-mediated mRNA decay and associate with major RNA-binding proteins (RBPs) such as Hfq and ProQ. If so, there must be additional sRNAs from mRNAs that accumulate only under specific physiological conditions. We test this prediction by characterizing candidate NarS that represents the 3' UTR of nitrate transporter NarK whose gene is silent during standard aerobic growth. We find that NarS acts by Hfq-dependent base pairing to repress the synthesis of the nitrite transporter, NirC, resulting in mRNA cross-regulation of nitrate and nitrite transporter genes. Interestingly, the NarS-mediated repression selectively targets the nirC cistron of the long nirBDC-cysG operon, an observation that we rationalize as a mechanism to protect the bacterial cytoplasm from excessive nitrite toxicity during anaerobic respiration with abundant nitrate. Our successful functional assignment of a 3' UTR sRNA from a non-standard growth condition supports the notion that mRNA crossregulation is more pervasive than currently appreciated. Abstract Small noncoding RNAs (sRNAs) from mRNA 3′ UTRs seem to present a previously unrecognized layer of bacterial post-transcriptional control whereby mRNAs influence each other's expression, independently of transcriptional control. Studies in Escherichia coli and Salmonella enterica showed that such sRNAs are natural products of RNase E-mediated mRNA decay and associate with major RNA-binding proteins (RBPs) such as Hfq and ProQ. If so, there must be additional sRNAs from mRNAs that accumulate only under specific physiological conditions. We test this prediction by characterizing candidate NarS that represents the 3′ UTR of nitrate transporter NarK whose gene is silent during standard aerobic growth. We find that NarS acts by Hfq-dependent base pairing to repress the synthesis of the nitrite transporter, NirC, resulting in mRNA cross-regulation of nitrate and nitrite transporter genes. Interestingly, the NarS-mediated repression selectively targets the nirC cistron of the long nirBDC-cysG operon, an observation that we rationalize as a mechanism to protect the bacterial cytoplasm from excessive nitrite toxicity during anaerobic respiration with abundant nitrate. Our successful functional assignment of a 3′ UTR sRNA from a non-standard growth condition supports the notion that mRNA crossregulation is more pervasive than currently appreciated. |
Author | Gao, Qian Matera, Gianluca Vogel, Jörg Chao, Yanjie Wang, Chuan |
AuthorAffiliation | 4 Helmholtz Institute for RNA-based Infection Research (HIRI) , Helmholtz Center for Infection Research (HZI), D-97080 Würzburg, Germany 3 Howard Hughes Medical Institute, Department of Molecular Biology and Microbiology, Tufts University School of Medicine , Boston, MA 02111, USA 2 Institute for Molecular Infection Biology, University of Würzburg , D-97080 Würzburg, Germany 1 Key Laboratory of Medical Molecular Virology (MOE/NHC/CAMS), School of Basic Medical Sciences, Shanghai Medical College, Fudan University , Shanghai 200033, PR China |
AuthorAffiliation_xml | – name: 2 Institute for Molecular Infection Biology, University of Würzburg , D-97080 Würzburg, Germany – name: 4 Helmholtz Institute for RNA-based Infection Research (HIRI) , Helmholtz Center for Infection Research (HZI), D-97080 Würzburg, Germany – name: 3 Howard Hughes Medical Institute, Department of Molecular Biology and Microbiology, Tufts University School of Medicine , Boston, MA 02111, USA – name: 1 Key Laboratory of Medical Molecular Virology (MOE/NHC/CAMS), School of Basic Medical Sciences, Shanghai Medical College, Fudan University , Shanghai 200033, PR China |
Author_xml | – sequence: 1 givenname: Chuan surname: Wang fullname: Wang, Chuan organization: Institute for Molecular Infection Biology, University of Würzburg, D-97080 Würzburg, Germany – sequence: 2 givenname: Yanjie surname: Chao fullname: Chao, Yanjie organization: Howard Hughes Medical Institute, Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, MA 02111, USA – sequence: 3 givenname: Gianluca surname: Matera fullname: Matera, Gianluca organization: Institute for Molecular Infection Biology, University of Würzburg, D-97080 Würzburg, Germany – sequence: 4 givenname: Qian surname: Gao fullname: Gao, Qian organization: Key Laboratory of Medical Molecular Virology (MOE/NHC/CAMS), School of Basic Medical Sciences, Shanghai Medical College, Fudan University, Shanghai 200033, PR China – sequence: 5 givenname: Jörg surname: Vogel fullname: Vogel, Jörg organization: Helmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Center for Infection Research (HZI), D-97080 Würzburg, Germany |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31863581$$D View this record in MEDLINE/PubMed |
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Commun. doi: 10.1038/ncomms8097 contributor: fullname: Fukuda |
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Snippet | Small noncoding RNAs (sRNAs) from mRNA 3' UTRs seem to present a previously unrecognized layer of bacterial post-transcriptional control whereby mRNAs... Abstract Small noncoding RNAs (sRNAs) from mRNA 3′ UTRs seem to present a previously unrecognized layer of bacterial post-transcriptional control whereby mRNAs... Small noncoding RNAs (sRNAs) from mRNA 3′ UTRs seem to present a previously unrecognized layer of bacterial post-transcriptional control whereby mRNAs... |
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SubjectTerms | 3' Untranslated Regions - genetics Anion Transport Proteins - genetics Endoribonucleases - genetics Escherichia coli - genetics Escherichia coli Proteins - genetics Gene Expression Regulation, Bacterial Host Factor 1 Protein - genetics Methyltransferases - genetics Nitrates - metabolism Operon - genetics Respiration - genetics RNA and RNA-protein complexes RNA Processing, Post-Transcriptional - genetics RNA Stability - genetics RNA, Messenger - genetics RNA, Small Untranslated - genetics RNA-Binding Proteins - genetics Salmonella enterica - genetics |
Title | The conserved 3' UTR-derived small RNA NarS mediates mRNA crossregulation during nitrate respiration |
URI | https://www.ncbi.nlm.nih.gov/pubmed/31863581 https://search.proquest.com/docview/2329729744 https://pubmed.ncbi.nlm.nih.gov/PMC7038943 |
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