RNA polymerase sliding on DNA can couple the transcription of nearby bacterial operons.


Journal

bioRxiv : the preprint server for biology
Titre abrégé: bioRxiv
Pays: United States
ID NLM: 101680187

Informations de publication

Date de publication:
10 Feb 2023
Historique:
entrez: 17 2 2023
pubmed: 18 2 2023
medline: 18 2 2023
Statut: epublish

Résumé

DNA transcription initiates after an RNA polymerase (RNAP) molecule binds to the promoter of a gene. In bacteria, the canonical picture is that RNAP comes from the cytoplasmic pool of freely diffusing RNAP molecules. Recent experiments suggest the possible existence of a separate pool of polymerases, competent for initiation, which freely slide on the DNA after having terminated one round of transcription. Promoter-dependent transcription reinitiation from this pool of post-termination RNAP may lead to coupled initiation at nearby operons, but it is unclear whether this can occur over the distance- and time-scales needed for it to function widely on a bacterial genome in vivo. Here, we mathematically model the hypothesized reinitiation mechanism as a diffusion-to-capture process and compute the distances over which significant inter-operon coupling can occur and the time required. These quantities depend on previously uncharacterized molecular association and dissociation rate constants between DNA, RNAP and the transcription initiation factor After transcribing an operon, a bacterial RNA polymerase can stay bound to DNA, slide along it, and reini-tiate transcription of the same or a different operon. Quantitative single-molecule biophysics experiments combined with mathematical theory demonstrate that this reinitiation process can be quick and efficient over gene spacings typical of a bacterial genome. Reinitiation may provide a mechanism to orchestrate the transcriptional activities of groups of nearby operons.

Identifiants

pubmed: 36798213
doi: 10.1101/2023.02.10.528045
pmc: PMC9934669
pii:
doi:

Types de publication

Preprint

Langues

eng

Commentaires et corrections

Type : UpdateIn

Références

Science. 2012 Jun 22;336(6088):1595-8
pubmed: 22723426
Nat Commun. 2015 Nov 13;6:8707
pubmed: 26566078
Nature. 1969 Jan 4;221(5175):43-6
pubmed: 4882047
Gene. 1996 Feb 2;168(1):31-5
pubmed: 8626061
Proc Natl Acad Sci U S A. 2010 Apr 6;107(14):6310-5
pubmed: 20308592
Genome Res. 2004 Jun;14(6):1060-7
pubmed: 15173112
RNA. 2008 Jan;14(1):170-9
pubmed: 18025254
Proc Natl Acad Sci U S A. 2015 Aug 11;112(32):E4390-9
pubmed: 26224838
Int J Mol Sci. 2021 Feb 27;22(5):
pubmed: 33673662
Nature. 1969 Aug 23;223(5208):854-5
pubmed: 4894964
Biophys J. 2018 May 8;114(9):2072-2082
pubmed: 29742401
J Bacteriol. 1994 Feb;176(4):1077-86
pubmed: 8106319
Elife. 2021 Feb 22;10:
pubmed: 33616038
Proc Natl Acad Sci U S A. 2017 Feb 14;114(7):E1081-E1090
pubmed: 28137878
J Biol Chem. 1998 Dec 4;273(49):32995-3001
pubmed: 9830052
Nat Struct Mol Biol. 2009 Dec;16(12):1224-9
pubmed: 19898474
Nat Commun. 2020 Jan 23;11(1):450
pubmed: 31974350
PLoS One. 2012;7(1):e29496
pubmed: 22235300
mBio. 2014 Jul 08;5(4):e01442-14
pubmed: 25006232
Mol Cell. 2021 Apr 1;81(7):1499-1514.e6
pubmed: 33621478
Proc Natl Acad Sci U S A. 2006 Apr 11;103(15):5752-7
pubmed: 16585517
Trends Genet. 2000 Mar;16(3):109-11
pubmed: 10689350
BMC Genomics. 2008 Jan 07;9:4
pubmed: 18179692
PLoS One. 2017 Apr 18;12(4):e0174887
pubmed: 28419102
Cell. 2012 Feb 17;148(4):679-89
pubmed: 22341441
Nat Commun. 2020 Jan 23;11(1):448
pubmed: 31974358
Nature. 2023 Jan;613(7945):783-789
pubmed: 36631609
Proc Natl Acad Sci U S A. 2006 Apr 4;103(14):5332-7
pubmed: 16567622
Nucleic Acids Res. 2000 Sep 15;28(18):3497-503
pubmed: 10982868
Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14294-9
pubmed: 10588699
Biotechnol J. 2010 Dec;5(12):1277-96
pubmed: 21154668
Biochemistry. 1976 Jul 27;15(15):3254-8
pubmed: 782516
Cell. 2005 Dec 16;123(6):1025-36
pubmed: 16360033
Methods. 2015 Sep 15;86:27-36
pubmed: 26032816
Annu Rev Microbiol. 2014;68:357-76
pubmed: 25002089
Science. 2012 Mar 2;335(6072):1103-6
pubmed: 22383849
Nat Rev Microbiol. 2016 Oct;14(10):638-50
pubmed: 27498839
PLoS One. 2008 Aug 20;3(8):e2981
pubmed: 18714358
Proc Natl Acad Sci U S A. 1987 Oct;84(20):7024-7
pubmed: 2823250
Nat Biotechnol. 2004 Jul;22(7):911-7
pubmed: 15229555
J Mol Biol. 1988 Jul 20;202(2):271-85
pubmed: 2459392

Auteurs

Debora Tenenbaum (D)

Department of Biochemistry, Brandeis University, Waltham, MA, United States.
Department of Physics, Brandeis University, Waltham, MA, United States.
Simons Center for Quantitative Biology, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.

Koe Inlow (K)

Department of Biochemistry, Brandeis University, Waltham, MA, United States.

Larry Friedman (L)

Department of Biochemistry, Brandeis University, Waltham, MA, United States.

Anthony Cai (A)

Department of Biochemistry, Brandeis University, Waltham, MA, United States.

Jeff Gelles (J)

Department of Biochemistry, Brandeis University, Waltham, MA, United States.

Jane Kondev (J)

Department of Physics, Brandeis University, Waltham, MA, United States.

Classifications MeSH