The conserved 3' UTR-derived small RNA NarS mediates mRNA crossregulation during nitrate respiration.

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 Nitrate Transporters Nitrates / metabolism Operon / genetics RNA Processing, Post-Transcriptional / genetics RNA Stability / genetics RNA, Messenger / genetics RNA, Small Untranslated / genetics RNA-Binding Proteins / genetics Respiration / genetics Salmonella enterica / genetics

Journal

Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011

Informations de publication

Date de publication:
28 02 2020
Historique:
accepted: 02 12 2019
revised: 27 11 2019
received: 15 08 2019
pubmed: 22 12 2019
medline: 19 3 2020
entrez: 22 12 2019
Statut: ppublish

Résumé

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.

Identifiants

DOI: 10.1093/nar/gkz1168 PMID: 31863581 PMC: PMC7038943
pubmed: 31863581
pii: 5682904
doi: 10.1093/nar/gkz1168
pmc: PMC7038943
doi:

Substances chimiques

3' Untranslated Regions 0
Anion Transport Proteins 0
Escherichia coli Proteins 0
Hfq protein, E coli 0
Host Factor 1 Protein 0
NirC protein, E coli 0
Nitrate Transporters 0
Nitrates 0
ProQ protein, E coli 0
RNA, Messenger 0
RNA, Small Untranslated 0
RNA-Binding Proteins 0
Methyltransferases EC 2.1.1.-
uroporphyrin-III C-methyltransferase EC 2.1.1.107
Endoribonucleases EC 3.1.-
ribonuclease E EC 3.1.4.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2126-2143

Informations de copyright

© The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research.

Références

Nucleic Acids Res. 2012 Apr;40(8):3623-40
pubmed: 22180532
Annu Rev Microbiol. 2016 Sep 8;70:25-44
pubmed: 27297126
Microbiology. 2016 Nov;162(11):1996-2004
pubmed: 27571709
Proc Natl Acad Sci U S A. 2013 Sep 10;110(37):E3487-96
pubmed: 23980183
Mol Cell. 2017 Jan 5;65(1):39-51
pubmed: 28061332
PLoS Biol. 2008 Mar 18;6(3):e64
pubmed: 18351803
Nucleic Acids Res. 2016 Aug 19;44(14):6935-48
pubmed: 27166377
mBio. 2016 Apr 05;7(2):e00312-16
pubmed: 27048800
Annu Rev Genet. 2014;48:537-59
pubmed: 25292357
Proc Natl Acad Sci U S A. 2016 Oct 11;113(41):11591-11596
pubmed: 27671629
Proc Natl Acad Sci U S A. 2001 Dec 18;98(26):15264-9
pubmed: 11742086
Nucleic Acids Res. 2007;35(3):1018-37
pubmed: 17264113
Curr Opin Microbiol. 2016 Feb;29:1-8
pubmed: 26426528
Nucleic Acids Res. 2008 May;36(8):2570-80
pubmed: 18334534
Genes Dev. 2014 Jul 15;28(14):1620-34
pubmed: 25030700
Mol Microbiol. 1988 Jul;2(4):527-30
pubmed: 2845227
Mol Microbiol. 2018 Nov;110(3):325-334
pubmed: 29995316
J Bacteriol. 1993 Jun;175(11):3259-68
pubmed: 8501030
J Bacteriol. 1991 Jun;173(11):3303-10
pubmed: 2045360
EMBO J. 2009 Jun 3;28(11):1551-61
pubmed: 19407815
EMBO J. 2012 Apr 18;31(8):1961-74
pubmed: 22388518
Nucleic Acids Res. 2003 Nov 15;31(22):6435-43
pubmed: 14602901
RNA. 2016 Mar;22(3):360-72
pubmed: 26759452
FEMS Microbiol Rev. 2015 May;39(3):316-30
pubmed: 25934118
Proc Natl Acad Sci U S A. 2011 Aug 9;108(32):13065-70
pubmed: 21737752
Genes Dev. 2009 Sep 1;23(17):2004-15
pubmed: 19638370
Cell. 2013 Apr 11;153(2):426-37
pubmed: 23582330
Proc Natl Acad Sci U S A. 2012 May 15;109(20):E1277-86
pubmed: 22538806
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W119-23
pubmed: 24838564
Elife. 2014 Dec 31;3:
pubmed: 25551292
Nucleic Acids Res. 2005 Feb 17;33(3):1040-50
pubmed: 15718303
Methods. 2017 Mar 15;117:67-76
pubmed: 27693881
FEBS Lett. 1993 Nov 29;335(1):57-60
pubmed: 8243665
Mol Microbiol. 2017 Jun;104(6):905-915
pubmed: 28370625
Genes Dev. 2005 Nov 1;19(21):2526-33
pubmed: 16264189
Nat Rev Microbiol. 2018 Oct;16(10):601-615
pubmed: 29995832
Mol Cell. 2018 Jun 7;70(5):971-982.e6
pubmed: 29804828
Sci STKE. 2003 Jun 03;2003(185):pe22
pubmed: 12783981
Biochem J. 1994 Sep 15;302 ( Pt 3):837-44
pubmed: 7945210
Biochemistry. 2015 Feb 10;54(5):1157-70
pubmed: 25582129
J Bacteriol. 1982 Sep;151(3):1320-5
pubmed: 7050087
Cell. 2018 Apr 19;173(3):749-761.e38
pubmed: 29606352
Mol Microbiol. 2010 Mar;75(5):1215-31
pubmed: 20070527
Proc Natl Acad Sci U S A. 2016 Jul 26;113(30):E4348-56
pubmed: 27407147
Mol Cell. 2016 Feb 4;61(3):352-363
pubmed: 26805574
Mol Microbiol. 2003 Nov;50(4):1111-24
pubmed: 14622403
Proc Natl Acad Sci U S A. 2015 Nov 10;112(45):E6243-52
pubmed: 26494284
Mol Cell. 2016 Sep 1;63(5):884-97
pubmed: 27588604
Bioinformatics. 2008 Mar 1;24(5):713-4
pubmed: 18227114
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
pubmed: 10829079
Annu Rev Microbiol. 2015;69:31-48
pubmed: 26002180
Biochem J. 1993 Dec 15;296 ( Pt 3):851-7
pubmed: 7506529
BMC Bioinformatics. 2011 Aug 04;12:323
pubmed: 21816040
Wiley Interdiscip Rev RNA. 2019 May;10(3):e1525
pubmed: 30761752
Nucleic Acids Res. 2019 Feb 28;47(4):2075-2088
pubmed: 30541135
Mol Microbiol. 2012 May;84(3):428-45
pubmed: 22458297
EMBO J. 2016 May 2;35(9):991-1011
pubmed: 27044921
EMBO J. 2017 Feb 1;36(3):374-387
pubmed: 27836995
Proc Natl Acad Sci U S A. 2019 Jan 15;116(3):1043-1052
pubmed: 30591570
Mol Cell. 2008 Dec 26;32(6):827-37
pubmed: 19111662
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Microbiol Spectr. 2018 Apr;6(2):
pubmed: 29676248
RNA. 2015 Apr;21(4):511-2
pubmed: 25780118
Curr Opin Microbiol. 2015 Apr;24:132-9
pubmed: 25677420
Mol Cell. 2011 Sep 16;43(6):880-91
pubmed: 21925377
EMBO J. 2012 Oct 17;31(20):4005-19
pubmed: 22922465
EMBO J. 2019 Aug 15;38(16):e101650
pubmed: 31313835
RNA Biol. 2013 Mar;10(3):337-41
pubmed: 23392245
Mol Cell. 2015 Jul 16;59(2):149-61
pubmed: 26186290
Nucleic Acids Res. 2019 Oct 10;47(18):9871-9887
pubmed: 31504767
Nat Rev Microbiol. 2013 Jan;11(1):45-57
pubmed: 23241849
Nat Methods. 2015 Apr;12(4):357-60
pubmed: 25751142
Mol Microbiol. 2007 Dec;66(5):1174-91
pubmed: 17971080
Mol Microbiol. 2007 Sep;65(6):1518-33
pubmed: 17824929
Mol Microbiol. 1992 Dec;6(23):3595-602
pubmed: 1474901
RNA. 2012 May;18(5):1062-74
pubmed: 22454537
Cell Host Microbe. 2013 Dec 11;14(6):683-95
pubmed: 24331466
Mol Microbiol. 2002 Apr;44(1):143-55
pubmed: 11967075
Eur J Biochem. 1990 Jul 31;191(2):325-31
pubmed: 2200673
EMBO J. 2015 Jun 3;34(11):1478-92
pubmed: 25630703
Curr Opin Microbiol. 2018 Apr;42:53-61
pubmed: 29125938
PLoS Genet. 2013 Jun;9(6):e1003565
pubmed: 23818864
Mol Microbiol. 1992 Oct;6(19):2805-13
pubmed: 1435259
J Biol Chem. 1978 Mar 10;253(5):1738-42
pubmed: 342528
EMBO J. 2017 Apr 13;36(8):1029-1045
pubmed: 28336682
Genes Dev. 2010 Dec 1;24(23):2621-6
pubmed: 21123649
RNA Biol. 2016 Oct 2;13(10):988-999
pubmed: 27420112
Mol Microbiol. 1997 Aug;25(3):583-95
pubmed: 9302020
RNA Biol. 2014;11(5):641-54
pubmed: 24922322
Nucleic Acids Res. 2014 Feb;42(3):2003-14
pubmed: 24234448
Biochem J. 1990 Feb 1;265(3):725-9
pubmed: 2407234
Nat Commun. 2015 May 11;6:7097
pubmed: 25959928
Nat Rev Microbiol. 2004 Jul;2(7):593-602
pubmed: 15197394

Auteurs

Chuan Wang (C)

Key Laboratory of Medical Molecular Virology (MOE/NHC/CAMS), School of Basic Medical Sciences, Shanghai Medical College, Fudan University, Shanghai 200033, PR China.
Institute for Molecular Infection Biology, University of Würzburg, D-97080 Würzburg, Germany.

Yanjie Chao (Y)

Institute for Molecular Infection Biology, University of Würzburg, D-97080 Würzburg, Germany.
Howard Hughes Medical Institute, Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, MA 02111, USA.

Gianluca Matera (G)

Institute for Molecular Infection Biology, University of Würzburg, D-97080 Würzburg, Germany.

Qian Gao (Q)

Key Laboratory of Medical Molecular Virology (MOE/NHC/CAMS), School of Basic Medical Sciences, Shanghai Medical College, Fudan University, Shanghai 200033, PR China.

Jörg Vogel (J)

Institute for Molecular Infection Biology, University of Würzburg, D-97080 Würzburg, Germany.
Helmholtz Institute for RNA-based Infection Research (HIRI), Helmholtz Center for Infection Research (HZI), D-97080 Würzburg, Germany.

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Classifications MeSH

questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Composants de génome › Gènes › Composants de gène › Régions non traduites › Régions 3' non traduites › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Protéines de transport membranaire › Pompes ioniques › Transporteurs d'anions › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Hydrolases › Esterases › Ribonucléases › Endoribonucleases › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Bactéries › Proteobacteria › Gammaproteobacteria › Enterobacteriaceae › Escherichia › Escherichia coli › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines bactériennes › Protéines Escherichia coli › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Régulation de l'expression des gènes bactériens › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Nucléoprotéines › Protéines de liaison à l'ARN › Protéine IHF-1 › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Transferases › One-carbon group transferases › Methyltransferases › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines végétales › Transporteurs de nitrate › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Composés chimiques organiques › Nitrates › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Génome microbien › Génome bactérien › Opéron › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Maturation post-transcriptionnelle des ARN › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Phénomènes chimiques › Phénomènes biochimiques › Stabilité de l'ARN › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ARN › ARN messager › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ARN › ARN non traduit › Petit ARN non traduit › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Nucléoprotéines › Protéines de liaison à l'ARN › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Phénomènes physiologiques respiratoires et circulatoires › Phénomènes physiologiques respiratoires › Respiration › The conserved 3' UTR-derived small RNA NarS...
questionsmedicales.fr › Bactéries › Proteobacteria › Gammaproteobacteria › Enterobacteriaceae › Salmonella › Salmonella enterica › The conserved 3' UTR-derived small RNA NarS...