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PreprintCited by 7Bacterial Genetics and BiotechnologyGenomics and Chromatin DynamicsRNA and protein synthesis mechanisms

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Template strand deoxyuridine promoter recognition by a viral RNA polymerase

Open access
Fraser, Alec, Sokolova, Maria L., Drobysheva, Arina V., Gordeeva, Julia V., Borukhov, Sergei, Artamonova, Tatyana O., AlphaFold team, Severinov, Konstantin V., Leiman, Petr G.·2021·Nature Communications
DOI 10.1101/2021.08.30.458274PMC PMC9209446

Preprint — published as 10.1038/s41467-022-31214-6 · Paper page

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Abstract

Bacillus subtilis bacteriophage AR9 employs two strategies for efficient host takeover control and host antiviral defense evasion – it encodes two unique DNA-dependent RNA polymerases (RNAPs) that function at different stages of virus morphogenesis in the cell, and its double stranded (ds) DNA genome contains uracils instead of thymines throughout 1,2 . Unlike any known RNAP, the AR9 non-virion RNAP (nvRNAP), which transcribes late phage genes, recognizes promoters in the template strand of dsDNA and efficiently differentiates obligatory uracils from thymines in its promoters 3 . Here, using structural data obtained by cryo-electron microscopy and X-ray crystallography on the AR9 nvRNAP core, holoenzyme, and a promoter complex, and a variety of in vitro transcription assays, we elucidate a unique mode of uracil-specific, template strand-dependent promoter recognition. It is achieved by a tripartite interaction between the promoter specificity subunit, the core enzyme, and DNA adopting a unique conformation. We also show that interaction with the non-template strand plays a critical role in the process of AR9 nvRNAP promoter recognition in dsDNA, and that the AR9 nvRNAP core and a part of its promoter specificity subunit that interacts with the core are structurally similar to their bacterial RNAP counterparts. Our work demonstrates the extent to which viruses can evolve new functional mechanisms to control acquired multisubunit cellular enzymes and make these enzymes serve their needs.

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Metadata

Authors
Fraser, A., Sokolova, M. L., Drobysheva, A. V., Gordeeva, J. V., Borukhov, S., Artamonova, T. O., AlphaFold team, Severinov, K. V., & Leiman, P. G.
Affiliations
  • The University of Texas Medical Branch at Galveston (US)
  • Skolkovo Institute of Science and Technology (RU)
  • Rowan University (US)
  • Peter the Great St. Petersburg Polytechnic University (RU)
  • Rutgers, The State University of New Jersey (US)
Corresponding author
  • Sokolova, Maria L.
  • Severinov, Konstantin V.
  • Leiman, Petr G.
ORCID
Venue
Nature Communications
Publisher
openRxiv
Published
2021-08-31
Volume
13
Issue
1
Pages
3526-3526
ISSN
2041-1723 (ISSN-L)
DOI
10.1101/2021.08.30.458274
PMC
PMC9209446
OpenAlex
W4283157815
Cited by
7
References
1
Citations by year
2026: 1 · 2025: 2 · 2024: 3 · 2023: 1
FWCI
0.91
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • Research Square (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Howard Hughes Medical Institute (DE-AC02-05CH11231)
  • U.S. Department of Energy (DE‐ AC02‐06CH11357, -AC02-05CH11231, Contract No. DE-AC02-06CH11357., Contract No. DE-AC02-05-CH11231, AC02‐06CH11357, 05CH11231, No. DE-AC02-05-CH11231, DE AC02 05CH11231, 085P1000817, 06CH11357, No. DE-AC02-06CH11357, DE-AC02-)
  • Michigan Economic Development Corporation (085P1000817, DE-AC02-06CH11357, Grant 085P1000817)
  • University of Texas Medical Branch
  • Russian Foundation for Basic Research (20-34-90079)
  • Russian Science Foundation (075-10-2021-114, 19-74-00011)
  • Skolkovo Institute of Science and Technology
  • National Institutes of Health (DE-AC02–05CH11231, DE-AC02–06CH11357, 085P1000817)
  • Office of Science (No. DE-AC02- 05-CH11231, Contract No. DE-AC02-06CH11357, AC02‐06CH11357, DEAC02–05CH11231, AC02-05CH11231, DE-AC02, No. DE-AC02-06CH11357., 085P1000817, 05CH11231, 06CH11357, Contract No. DE-AC02-05CH11231, DE-AC02-06CH11357)
  • Department of Mechanical Engineering, University of Texas at Austin
  • Michigan Technology Tri-Corridor (DE-AC02-06CH11357, 085P1000817, DE-AC02-05CH11231)
  • Simons Center for the Social Brain, Massachusetts Institute of Technology
  • National Institute of General Medical Sciences (R01GM139034, R01GM130942)
  • Argonne National Laboratory (DE- AC02-06-CH11357, DE-AC02, AC02–06CH11357, 085P1000817, DE-AC02-05CH11231, No. DE-AC02-06CH11357, 06CH11357, Contract No. DE-AC02-06CH11357.)
  • SLAC National Accelerator Laboratory (DE-AC02-05-CH11231, DE-AC02-06CH11357)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
Keywords
sigma factor, promoter identification, deoxyuridine, template strand, transcription initiation
MeSH terms
Viral Replicase Complex Proteins, Deoxyuridine, Promoter Regions, Genetic, DNA-Directed RNA Polymerases, RNA, Viral, Sigma Factor, Transcription, Genetic

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