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Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail

Author

Listed:
  • Anastasiia Chaban

    (Center of Life Sciences, Skolkovo Institute of Science and Technology
    RIKEN Center for Biosystems Dynamics Research
    Structural and Computational Biology Unit, European Molecular Biology Laboratory (EMBL))

  • Leonid Minakhin

    (The State University of New Jersey
    Thomas Jefferson University)

  • Ekaterina Goldobina

    (Center of Life Sciences, Skolkovo Institute of Science and Technology
    University College Cork)

  • Brain Bae

    (University of Illinois at Urbana−Champaign)

  • Yue Hao

    (University of Illinois at Urbana−Champaign)

  • Sergei Borukhov

    (Rowan University School of Osteopathic Medicine at Stratford)

  • Leena Putzeys

    (Laboratory of Gene Technology, KU Leuven)

  • Maarten Boon

    (Laboratory of Gene Technology, KU Leuven)

  • Florian Kabinger

    (Max Planck Institute for Multidisciplinary Sciences)

  • Rob Lavigne

    (Laboratory of Gene Technology, KU Leuven)

  • Kira S. Makarova

    (National Institutes of Health)

  • Eugene V. Koonin

    (National Institutes of Health)

  • Satish K. Nair

    (University of Illinois at Urbana−Champaign)

  • Shunsuke Tagami

    (RIKEN Center for Biosystems Dynamics Research)

  • Konstantin Severinov

    (The State University of New Jersey
    Institute of Molecular Genetics National Kurchatov Center)

  • Maria L. Sokolova

    (Center of Life Sciences, Skolkovo Institute of Science and Technology
    Max Planck Institute for Multidisciplinary Sciences)

Abstract

Thermus thermophilus bacteriophage P23-45 encodes a giant 5,002-residue tail tape measure protein (TMP) that defines the length of its extraordinarily long tail. Here, we show that the N-terminal portion of P23-45 TMP is an unusual RNA polymerase (RNAP) homologous to cellular RNAPs. The TMP-fused virion RNAP transcribes pre-early phage genes, including a gene that encodes another, non-virion RNAP, that transcribes early and some middle phage genes. We report the crystal structures of both P23-45 RNAPs. The non-virion RNAP has a crab-claw-like architecture. By contrast, the virion RNAP adopts a unique flat structure without a clamp. Structure and sequence comparisons of the P23-45 RNAPs with other RNAPs suggest that, despite the extensive functional differences, the two P23-45 RNAPs originate from an ancient gene duplication in an ancestral phage. Our findings demonstrate striking adaptability of RNAPs that can be attained within a single virus species.

Suggested Citation

  • Anastasiia Chaban & Leonid Minakhin & Ekaterina Goldobina & Brain Bae & Yue Hao & Sergei Borukhov & Leena Putzeys & Maarten Boon & Florian Kabinger & Rob Lavigne & Kira S. Makarova & Eugene V. Koonin , 2024. "Tail-tape-fused virion and non-virion RNA polymerases of a thermophilic virus with an extremely long tail," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44630-z
    DOI: 10.1038/s41467-023-44630-z
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    References listed on IDEAS

    as
    1. David Forrest & Katherine James & Yulia Yuzenkova & Nikolay Zenkin, 2017. "Single-peptide DNA-dependent RNA polymerase homologous to multi-subunit RNA polymerase," Nature Communications, Nature, vol. 8(1), pages 1-8, August.
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