Comprehensive transcription terminator atlas for Bacillus subtilis.


Journal

Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869

Informations de publication

Date de publication:
11 2022
Historique:
received: 13 01 2022
accepted: 26 08 2022
pubmed: 4 10 2022
medline: 1 11 2022
entrez: 3 10 2022
Statut: ppublish

Résumé

The transcriptome-wide contributions of Rho-dependent and intrinsic (Rho-independent) transcription termination mechanisms in bacteria are unclear. By sequencing released transcripts in a wild-type strain and strains containing deficiencies in NusA, NusG and/or Rho (10 strains), we produced an atlas of terminators for the model Gram-positive bacterium Bacillus subtilis. We found that NusA and NusG stimulate 77% and 19% of all intrinsic terminators, respectively, and that both proteins participate in Rho-dependent termination. We also show that Rho stimulates termination at 10% of the intrinsic terminators in vivo. We recapitulated Rho-stimulated intrinsic termination at 5 terminators in vitro and found that Rho requires the KOW domain of NusG to stimulate this process at one of these terminators. Computational analyses of our atlas using RNAstructure, MEME suite and DiffLogo, combined with in vitro transcription experiments, revealed that Rho stimulates intrinsic terminators with weak hairpins and/or U-rich tracts by remodelling the RNA upstream of the intrinsic terminator to prevent the formation of RNA structures that could otherwise compete with the terminator hairpin. We also identified 56 putative examples of 'hybrid Rho-dependent termination', wherein classical Rho-dependent termination occurs after readthrough of a Rho-stimulated intrinsic terminator.

Identifiants

pubmed: 36192538
doi: 10.1038/s41564-022-01240-7
pii: 10.1038/s41564-022-01240-7
pmc: PMC10024249
mid: NIHMS1875971
doi:

Substances chimiques

RNA 63231-63-0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1918-1931

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM098399
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM131860
Pays : United States

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature Limited.

Références

J Mol Biol. 2019 Sep 20;431(20):4030-4039
pubmed: 30978344
J Biol Chem. 1983 Jul 10;258(13):8146-50
pubmed: 6345540
Mol Cell. 1999 Apr;3(4):495-504
pubmed: 10230402
Proc Natl Acad Sci U S A. 2008 Oct 21;105(42):16131-6
pubmed: 18852477
Proc Natl Acad Sci U S A. 1981 May;78(5):2913-7
pubmed: 6265923
Proc Natl Acad Sci U S A. 1982 Oct;79(20):6171-5
pubmed: 6216477
Nature. 2020 Sep;585(7823):124-128
pubmed: 32848247
J Mol Biol. 1976 Sep 15;106(2):231-41
pubmed: 135845
RNA. 2020 Oct;26(10):1431-1447
pubmed: 32611709
Mol Cell. 2004 Apr 9;14(1):117-26
pubmed: 15068808
J Biol Chem. 1987 Aug 15;262(23):11292-9
pubmed: 3038914
BMC Bioinformatics. 2010 Mar 15;11:129
pubmed: 20230624
Mol Microbiol. 1999 Jan;31(2):651-63
pubmed: 10027981
Science. 2021 Jan 1;371(6524):
pubmed: 33243850
Cell. 2003 Jul 11;114(1):135-46
pubmed: 12859904
Nat Microbiol. 2016 Jan 11;1:15007
pubmed: 27571753
Proc Natl Acad Sci U S A. 1978 Oct;75(10):4828-32
pubmed: 154103
Cell. 1992 Mar 6;68(5):989-94
pubmed: 1547498
Nucleic Acids Res. 2016 Apr 20;44(7):3364-72
pubmed: 26857544
Cell. 2005 Jan 14;120(1):49-58
pubmed: 15652481
J Biol Chem. 2016 Mar 4;291(10):5299-308
pubmed: 26742846
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Genome Biol. 2014;15(12):550
pubmed: 25516281
Nat Biotechnol. 2016 May;34(5):525-7
pubmed: 27043002
Cell. 1982 Jul;29(3):945-51
pubmed: 6758952
Annu Rev Biochem. 2016 Jun 2;85:319-47
pubmed: 27023849
Proc Natl Acad Sci U S A. 2006 Mar 28;103(13):4870-5
pubmed: 16551743
Nat Rev Microbiol. 2011 May;9(5):319-29
pubmed: 21478900
J Bacteriol. 2022 May 17;204(5):e0053421
pubmed: 35258320
J Bacteriol. 2004 Jan;186(2):278-86
pubmed: 14702295
mBio. 2022 Apr 26;13(2):e0040022
pubmed: 35311531
J Mol Biol. 2011 Oct 7;412(5):793-813
pubmed: 21439297
Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1453-7
pubmed: 1741399
Proc Int Conf Intell Syst Mol Biol. 1994;2:28-36
pubmed: 7584402
J Mol Biol. 1990 May 5;213(1):79-108
pubmed: 1692594
iScience. 2021 Oct 23;24(11):103333
pubmed: 34805793
Structure. 2005 Jan;13(1):99-109
pubmed: 15642265
Science. 2010 Apr 23;328(5977):501-4
pubmed: 20413501
Mol Cell. 2021 Jan 21;81(2):281-292.e8
pubmed: 33296676
Cell. 2018 Apr 19;173(3):749-761.e38
pubmed: 29606352
RNA Biol. 2021 Nov;18(11):1692-1701
pubmed: 33323028
J Bacteriol. 2012 Apr;194(7):1697-707
pubmed: 22307755
Nat Methods. 2013 Jul;10(7):659-64
pubmed: 23727987
Anal Biochem. 1979 Nov 15;100(1):95-7
pubmed: 161695
Proc Natl Acad Sci U S A. 2019 Mar 5;116(10):4440-4445
pubmed: 30782818
Elife. 2019 Jan 08;8:
pubmed: 30618376
Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):15908-13
pubmed: 12456892
Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8793-7
pubmed: 7568019
PLoS Genet. 2017 Jul 19;13(7):e1006909
pubmed: 28723971
Mol Cell. 2002 Nov;10(5):1151-62
pubmed: 12453422
Biochim Biophys Acta. 2002 Sep 13;1577(2):251-260
pubmed: 12213656
Proc Natl Acad Sci U S A. 2020 Sep 1;117(35):21628-21636
pubmed: 32817529
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Proc Natl Acad Sci U S A. 2002 Aug 20;99(17):11067-72
pubmed: 12161562
Elife. 2021 Apr 09;10:
pubmed: 33835023
Nucleic Acids Res. 2018 Jul 27;46(13):6797-6805
pubmed: 29669055
Nat Microbiol. 2019 Nov;4(11):1907-1918
pubmed: 31308523
Mol Cell. 2018 Mar 1;69(5):816-827.e4
pubmed: 29499136
Bioinformatics. 2010 Mar 15;26(6):841-2
pubmed: 20110278
J Biol Chem. 1984 Sep 25;259(18):11550-5
pubmed: 6206069
BMC Bioinformatics. 2015 Nov 17;16:387
pubmed: 26577052
Nucleic Acids Res. 2018 Sep 19;46(16):8245-8260
pubmed: 29931073
Science. 2016 Apr 8;352(6282):aad9822
pubmed: 27120414
Science. 2001 Apr 27;292(5517):730-3
pubmed: 11326100
Nucleic Acids Res. 1978 Dec;5(12):4613-23
pubmed: 370776

Auteurs

Zachary F Mandell (ZF)

Department of Biochemistry and Molecular Biology, Center for RNA Molecular Biology, Pennsylvania State University, University Park, PA, USA.
Department of Molecular Biology and Genetics and Department of Biology, Johns Hopkins University, Baltimore, MD, USA.

Rishi K Vishwakarma (RK)

Department of Biochemistry and Molecular Biology, Center for RNA Molecular Biology, Pennsylvania State University, University Park, PA, USA.

Helen Yakhnin (H)

Department of Biochemistry and Molecular Biology, Center for RNA Molecular Biology, Pennsylvania State University, University Park, PA, USA.

Katsuhiko S Murakami (KS)

Department of Biochemistry and Molecular Biology, Center for RNA Molecular Biology, Pennsylvania State University, University Park, PA, USA.

Mikhail Kashlev (M)

NCI RNA Biology Laboratory, Center for Cancer Research, NCI, Frederick, MD, USA.

Paul Babitzke (P)

Department of Biochemistry and Molecular Biology, Center for RNA Molecular Biology, Pennsylvania State University, University Park, PA, USA. pxb28@psu.edu.

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Classifications MeSH