Structure of a bacterial RNA polymerase holoenzyme open promoter complex

Bae, Brian; Feklistov, Andrey; Lass-Napiorkowska, Agnieszka; Landick, Robert; Darst, Seth A.

doi:10.7554/eLife.08504

Title: Structure of a bacterial RNA polymerase holoenzyme open promoter complex

Journal Article · Tue Sep 08 00:00:00 EDT 2015 · eLife

DOI:https://doi.org/10.7554/eLife.08504· OSTI ID:1354557

Bae, Brian ^[1]; Feklistov, Andrey ^[1]; Lass-Napiorkowska, Agnieszka ^[2]; Landick, Robert ^[3]; Darst, Seth A. ^[1]

Laboratory for Molecular Biophysics, The Rockefeller University, New York, United States
Edward A. Doisy Department of Biochemistry and Molecular Biology, Saint Louis University School of Medicine, St Louis, United States
Department of Biochemistry, University of Wisconsin-madison, Madison, United States; Department of Bacteriology, University of Wisconsin-Madison, Madison, United States

Initiation of transcription is a primary means for controlling gene expression. In bacteria, the RNA polymerase (RNAP) holoenzyme binds and unwinds promoter DNA, forming the transcription bubble of the open promoter complex (RPo). We have determined crystal structures, refined to 4.14 Å-resolution, of RPo containing Thermus aquaticus RNAP holoenzyme and promoter DNA that includes the full transcription bubble. The structures, combined with biochemical analyses, reveal key features supporting the formation and maintenance of the double-strand/single-strand DNA junction at the upstream edge of the -10 element where bubble formation initiates. The results also reveal RNAP interactions with duplex DNA just upstream of the -10 element and potential protein/DNA interactions that direct the DNA template strand into the RNAP active site. Addition of an RNA primer to yield a 4 base-pair post-translocated RNA:DNA hybrid mimics an initially transcribing complex at the point where steric clash initiates abortive initiation and σA dissociation.

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Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

DOE Contract Number:: SC00112704

OSTI ID:: 1354557

Report Number(s):: BNL-113074-2016-JA

Journal Information:: eLife, Vol. 4; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.

Country of Publication:: United States

Language:: English

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E. coli TraR allosterically regulates transcription initiation by altering RNA polymerase conformation Chen, James; Gopalkrishnan, Saumya; Chiu, Courtney eLife, Vol. 8 https://doi.org/10.7554/elife.49375	journal	December 2019
Characterizing highly dynamic conformational states: The transcription bubble in RNAP-promoter open complex as an example Lerner, Eitan; Ingargiola, Antonino; Weiss, Shimon The Journal of Chemical Physics, Vol. 148, Issue 12 https://doi.org/10.1063/1.5004606	journal	March 2018
Structural basis of transcription activation Feng, Y.; Zhang, Y.; Ebright, R. H. Science, Vol. 352, Issue 6291 https://doi.org/10.1126/science.aaf4417	journal	June 2016
The universally-conserved transcription factor RfaH is recruited to a hairpin structure of the non-template DNA strand Zuber, Philipp K.; Artsimovitch, Irina; NandyMazumdar, Monali eLife, Vol. 7 https://doi.org/10.7554/elife.36349	journal	May 2018
Active site closure stabilizes the backtracked state of RNA polymerase Turtola, Matti; Mäkinen, Janne J.; Belogurov, Georgiy A. Nucleic Acids Research https://doi.org/10.1101/410746	journal	September 2018
Structural basis of transcription inhibition by the DNA mimic protein Ocr of bacteriophage T7 Ye, Fuzhou; Kotta-Loizou, Ioly; Jovanovic, Milija eLife https://doi.org/10.1101/822460	journal	October 2019
Reaction Mechanisms of Pol IV, RDR2, and DCL3 Drive RNA Channeling in the siRNA-Directed DNA Methylation Pathway Singh, Jasleen; Mishra, Vibhor; Wang, Feng Molecular Cell, Vol. 75, Issue 3 https://doi.org/10.1016/j.molcel.2019.07.008	journal	August 2019
Structures and mechanism of transcription initiation by bacterial ECF factors Fang, Chengli; Li, Lingting; Shen, Liqiang Nucleic Acids Research, Vol. 47, Issue 13 https://doi.org/10.1093/nar/gkz470	journal	May 2019
RNA polymerase motions during promoter melting Feklistov, Andrey; Bae, Brian; Hauver, Jesse Science, Vol. 356, Issue 6340 https://doi.org/10.1126/science.aam7858	journal	May 2017
Structural basis of ECF-σ-factor-dependent transcription initiation Lin, Wei; Mandal, Sukhendu; Degen, David Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08443-3	journal	February 2019
Transcription initiation complex structures elucidate DNA opening Plaschka, C.; Hantsche, M.; Dienemann, C. Nature, Vol. 533, Issue 7603 https://doi.org/10.1038/nature17990	journal	May 2016
Structural basis of σ appropriation Shi, Jing; Wen, Aijia; Zhao, Minxing Nucleic Acids Research, Vol. 47, Issue 17 https://doi.org/10.1093/nar/gkz682	journal	August 2019
Target preference of Type III-A CRISPR-Cas complexes at the transcription bubble Liu, Tina Y.; Liu, Jun-Jie; Aditham, Abhishek J. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10780-2	journal	July 2019
Fidaxomicin jams Mycobacterium tuberculosis RNA polymerase motions needed for initiation via RbpA contacts Boyaci, Hande; Chen, James; Lilic, Mirjana eLife, Vol. 7 https://doi.org/10.7554/elife.34823	journal	February 2018
High-throughput detection of RNA processing in bacteria Gill, Erin E.; Chan, Luisa S.; Winsor, Geoffrey L. BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-4538-8	journal	March 2018
Enhanced basepair dynamics pre-disposes protein-assisted flips of key bases in DNA strand separation during transcription initiation Roy, Neeladri Sekhar; Debnath, Subrata; Chakraborty, Abhijit Physical Chemistry Chemical Physics, Vol. 20, Issue 14 https://doi.org/10.1039/c8cp01119b	journal	January 2018
Active site closure stabilizes the backtracked state of RNA polymerase Turtola, Matti; Mäkinen, Janne J.; Belogurov, Georgiy A. Nucleic Acids Research https://doi.org/10.1093/nar/gky883	journal	September 2018
Structures of E . coli σ ^S -transcription initiation complexes provide new insights into polymerase mechanism Liu, Bin; Zuo, Yuhong; Steitz, Thomas A. Proceedings of the National Academy of Sciences, Vol. 113, Issue 15 https://doi.org/10.1073/pnas.1520555113	journal	March 2016
Transcription initiation in mycobacteria: a biophysical perspective Boyaci, Hande; Saecker, Ruth M.; Campbell, Elizabeth A. Transcription, Vol. 11, Issue 2 https://doi.org/10.1080/21541264.2019.1707612	journal	December 2019
Where to begin? Sigma factors and the selectivity of transcription initiation in bacteria Helmann, John D. Molecular Microbiology, Vol. 112, Issue 2 https://doi.org/10.1111/mmi.14309	journal	June 2019
Ancient Transcription Factors in the News Artsimovitch, Irina; Knauer, Stefan H. mBio, Vol. 10, Issue 1 https://doi.org/10.1128/mbio.01547-18	journal	February 2019
The universally-conserved transcription factor RfaH is recruited to a hairpin structure of the non-template DNA strand Zuber, Philipp K.; Artsimovitch, Irina; Mazumdar, Monali Nandy eLife https://doi.org/10.1101/264887	journal	April 2018

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