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

Tenenbaum, Debora, Inlow, Koe, Friedman, Larry J, Cai, Anthony, Gelles, Jeff, Kondev, Jane (July 2023) RNA polymerase sliding on DNA can couple the transcription of nearby bacterial operons. Proceedings of the National Academy of Sciences of USA, 120 (30). e2301402120. ISSN 0027-8424

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Abstract

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 posttermination RNAP may lead to coupled initiation at nearby operons, but it is unclear whether this can occur over the distance and timescales 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 interoperon coupling can occur and the time required. These quantities depend on molecular association and dissociation rate constants between DNA, RNAP, and the transcription initiation factor σ70; we measure these rate constants using single-molecule experiments in vitro. Our combined theory/experimental results demonstrate that efficient coupling can occur at physiologically relevant σ70 concentrations and on timescales appropriate for transcript synthesis. Coupling is efficient over terminator-promoter distances up to ∼1,000 bp, which includes the majority of terminator-promoter nearest neighbor pairs in the Escherichia coli genome. The results suggest a generalized mechanism that couples the transcription of nearby operons and breaks the paradigm that each binding of RNAP to DNA can produce at most one messenger RNA.

Item Type:	Paper
Subjects:	bioinformatics bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification > transcription bioinformatics > genomics and proteomics > genetics & nucleic acid processing bioinformatics > genomics and proteomics bioinformatics > genomics and proteomics > genetics & nucleic acid processing > protein structure, function, modification > protein types > enzymes > RNA polymerase organism description > bacteria organism description > bacteria > escherichia coli bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification > operons
CSHL Authors:	Tenenbaum, Debora
Communities:	CSHL labs > Kinney lab
SWORD Depositor:	CSHL Elements
Depositing User:	CSHL Elements
Date:	25 July 2023
Date Deposited:	20 Sep 2023 18:07
Last Modified:	11 Jan 2024 14:35
PMCID:	PMC10372574
Related URLs:	Publisher
URI:	https://repository.cshl.edu/id/eprint/40930

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