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An anionic ligand snap-locks a long-range interaction in a magnesium-folded riboswitch

Author

Listed:
  • Rajeev Yadav

    (University of Michigan
    Michigan State University)

  • Julia R. Widom

    (University of Michigan
    University of Oregon)

  • Adrien Chauvier

    (University of Michigan)

  • Nils G. Walter

    (University of Michigan)

Abstract

The archetypical transcriptional crcB fluoride riboswitch from Bacillus cereus is an intricately structured non-coding RNA element enhancing gene expression in response to toxic levels of fluoride. Here, we used single molecule FRET to uncover three dynamically interconverting conformations appearing along the transcription process: two distinct undocked states and one pseudoknotted docked state. We find that the fluoride anion specifically snap-locks the magnesium-induced, dynamically docked state. The long-range, nesting, single base pair A40-U48 acts as the main linchpin, rather than the multiple base pairs comprising the pseudoknot. We observe that the proximally paused RNA polymerase further fine-tunes the free energy to promote riboswitch docking. Finally, we show that fluoride binding at short transcript lengths is an early step toward partitioning folding into the docked conformation. These results reveal how the anionic fluoride ion cooperates with the magnesium-associated RNA to govern regulation of downstream genes needed for fluoride detoxification of the cell.

Suggested Citation

  • Rajeev Yadav & Julia R. Widom & Adrien Chauvier & Nils G. Walter, 2022. "An anionic ligand snap-locks a long-range interaction in a magnesium-folded riboswitch," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-021-27827-y
    DOI: 10.1038/s41467-021-27827-y
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    Cited by:

    1. Adrien Chauvier & Shiba S. Dandpat & Rosa Romero & Nils G. Walter, 2024. "A nascent riboswitch helix orchestrates robust transcriptional regulation through signal integration," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Courtney E. Szyjka & Eric J. Strobel, 2023. "Observation of coordinated RNA folding events by systematic cotranscriptional RNA structure probing," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    3. Xiaolin Niu & Zhonghe Xu & Yufan Zhang & Xiaobing Zuo & Chunlai Chen & Xianyang Fang, 2023. "Structural and dynamic mechanisms for coupled folding and tRNA recognition of a translational T-box riboswitch," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Yanyan Xue & Jun Li & Dian Chen & Xizhu Zhao & Liang Hong & Yu Liu, 2023. "Observation of structural switch in nascent SAM-VI riboswitch during transcription at single-nucleotide and single-molecule resolution," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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