A Mn-sensing riboswitch activates expression of a Mn2+/Ca2+ ATPase transporter in Streptococcus.
Adenosine Triphosphatases
/ biosynthesis
Aptamers, Nucleotide
Bacillus subtilis
/ genetics
Bacterial Proteins
/ biosynthesis
Calcium
/ pharmacology
Gene Expression Regulation, Bacterial
Homeostasis
Manganese
/ metabolism
Membrane Transport Proteins
/ biosynthesis
Nucleic Acid Conformation
/ drug effects
RNA, Bacterial
/ genetics
Riboswitch
Streptococcus pneumoniae
/ genetics
Journal
Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011
Informations de publication
Date de publication:
26 07 2019
26 07 2019
Historique:
accepted:
31
05
2019
revised:
08
05
2019
received:
21
03
2019
pubmed:
6
6
2019
medline:
7
1
2020
entrez:
6
6
2019
Statut:
ppublish
Résumé
Maintaining manganese (Mn) homeostasis is important for the virulence of numerous bacteria. In the human respiratory pathogen Streptococcus pneumoniae, the Mn-specific importer PsaBCA, exporter MntE, and transcriptional regulator PsaR establish Mn homeostasis. In other bacteria, Mn homeostasis is controlled by yybP-ykoY family riboswitches. Here, we characterize a yybP-ykoY family riboswitch upstream of the mgtA gene encoding a PII-type ATPase in S. pneumoniae, suggested previously to function in Ca2+ efflux. We show that the mgtA riboswitch aptamer domain adopts a canonical yybP-ykoY structure containing a three-way junction that is compacted in the presence of Ca2+ or Mn2+ at a physiological Mg2+ concentration. Although Ca2+ binds to the RNA aptamer with higher affinity than Mn2+, in vitro activation of transcription read-through of mgtA by Mn2+ is much greater than by Ca2+. Consistent with this result, mgtA mRNA and protein levels increase ≈5-fold during cellular Mn stress, but only in genetic backgrounds of S. pneumoniae and Bacillus subtilis that exhibit Mn2+ sensitivity, revealing that this riboswitch functions as a failsafe 'on' signal to prevent Mn2+ toxicity in the presence of high cellular Mn2+. In addition, our results suggest that the S. pneumoniae yybP-ykoY riboswitch functions to regulate Ca2+ efflux under these conditions.
Identifiants
pubmed: 31165873
pii: 5511479
doi: 10.1093/nar/gkz494
pmc: PMC6649816
doi:
Substances chimiques
Aptamers, Nucleotide
0
Bacterial Proteins
0
Membrane Transport Proteins
0
RNA, Bacterial
0
Riboswitch
0
Manganese
42Z2K6ZL8P
Adenosine Triphosphatases
EC 3.6.1.-
MgtA protein, bacteria
EC 3.6.1.-
Calcium
SY7Q814VUP
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
6885-6899Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM127715
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM118157
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM131767
Pays : United States
Informations de copyright
© The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research.
Références
Cell Chem Biol. 2018 Aug 16;25(8):962-973.e5
pubmed: 29805037
Mol Microbiol. 2008 Oct;70(2):435-44
pubmed: 18761687
Front Cell Infect Microbiol. 2015 Jan 13;4:194
pubmed: 25629011
J Biol Chem. 2014 Jul 25;289(30):20492-501
pubmed: 24917681
RNA Biol. 2011 Jan-Feb;8(1):5-10
pubmed: 21317561
Front Immunol. 2016 Oct 18;7:431
pubmed: 27803700
Nat Chem Biol. 2019 Mar;15(3):241-249
pubmed: 30692683
Nat Rev Microbiol. 2018 Jun;16(6):355-367
pubmed: 29599457
Mol Microbiol. 2013 Feb;87(3):466-77
pubmed: 23171030
Mol Microbiol. 2017 Jan;103(2):253-268
pubmed: 27748968
Nature. 2017 Nov 16;551(7680):346-351
pubmed: 29144454
Biochemistry. 2013 Oct 29;52(43):7689-701
pubmed: 24067066
PLoS Pathog. 2011 Sep;7(9):e1002261
pubmed: 21980287
Cell. 2009 Feb 20;136(4):615-28
pubmed: 19239884
Nat Protoc. 2006;1(3):1610-6
pubmed: 17406453
Mol Microbiol. 2019 Mar;111(3):764-783
pubmed: 30582886
J Bacteriol. 2016 Jan 19;198(7):1066-76
pubmed: 26787764
Adv Genet. 2015;90:133-208
pubmed: 26296935
J Am Chem Soc. 2007 Apr 11;129(14):4144-5
pubmed: 17367143
Nucleic Acids Res. 2012 Apr;40(7):3117-30
pubmed: 22139931
Biophys J. 1999 Jun;76(6):2879-86
pubmed: 10354416
Mol Biol Cell. 1998 May;9(5):1149-62
pubmed: 9571246
Proc Natl Acad Sci U S A. 2012 May 15;109(20):E1277-86
pubmed: 22538806
Nucleic Acids Res. 2018 Nov 2;46(19):9971-9989
pubmed: 30107613
Annu Rev Microbiol. 2004;58:303-28
pubmed: 15487940
Lancet. 2009 Sep 12;374(9693):893-902
pubmed: 19748398
Proc Natl Acad Sci U S A. 2004 Apr 27;101(17):6421-6
pubmed: 15096624
Methods. 2010 Oct;52(2):180-91
pubmed: 20554045
Cell. 2007 Sep 7;130(5):878-92
pubmed: 17803910
J Bacteriol. 2011 Nov;193(21):5887-97
pubmed: 21908668
Mol Cell. 2015 Mar 19;57(6):1110-1123
pubmed: 25794619
Mol Microbiol. 2009 Apr;72(1):12-25
pubmed: 19226324
Proc Natl Acad Sci U S A. 2011 Jan 11;108(2):858-63
pubmed: 21187401
Front Cell Infect Microbiol. 2013 Dec 04;3:92
pubmed: 24364001
Infect Immun. 2011 Jun;79(6):2314-23
pubmed: 21422174
Nat Chem Biol. 2017 Oct;13(10):1109-1114
pubmed: 28825710
Mol Cell. 2011 Sep 16;43(6):880-91
pubmed: 21925377
Crit Rev Biochem Mol Biol. 2005 Mar-Apr;40(2):93-113
pubmed: 15814430
Nature. 2012 May 13;486(7401):85-9
pubmed: 22678284
RNA. 2007 Aug;13(8):1256-67
pubmed: 17585050
J Mol Biol. 2009 Sep 25;392(3):723-35
pubmed: 19619558
J Biol Chem. 2005 Jun 17;280(24):22800-8
pubmed: 15831496
Lancet Infect Dis. 2018 Nov;18(11):1191-1210
pubmed: 30243584
Nucleic Acid Ther. 2012 Jun;22(3):177-86
pubmed: 22468692
Nat Struct Biol. 2003 Aug;10(8):652-7
pubmed: 12847518
Methods Enzymol. 2000;317:368-93
pubmed: 10829291
FEMS Microbiol Rev. 2014 Nov;38(6):1235-49
pubmed: 25211180
Mol Microbiol. 2000 Mar;35(6):1454-68
pubmed: 10760146
J Bacteriol. 2010 Jan;192(1):264-79
pubmed: 19854910
Future Microbiol. 2009 Feb;4(1):85-103
pubmed: 19207102
PLoS One. 2012;7(5):e37294
pubmed: 22629378
Biol Cell. 2009 Feb;101(2):117-31
pubmed: 19076068
BMC Genomics. 2010 Jun 03;11:350
pubmed: 20525227
Nat Commun. 2017 Dec 1;8(1):1884
pubmed: 29192165
J Phys Chem B. 2019 Mar 7;123(9):2005-2015
pubmed: 30739441
Nucleic Acids Res. 2006;34(12):3484-93
pubmed: 16870723
Mol Microbiol. 2017 Apr;104(2):334-348
pubmed: 28127804
RNA. 2012 Mar;18(3):530-46
pubmed: 22274957
Mol Cell. 2015 Mar 19;57(6):1099-1109
pubmed: 25794618
RNA. 2013 Jan;19(1):63-73
pubmed: 23188808
Methods Enzymol. 2014;549:165-87
pubmed: 25432749