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Structural insights into the Venus flytrap mechanosensitive ion channel Flycatcher1

Author

Listed:
  • Sebastian Jojoa-Cruz

    (Department of Integrative Structural and Computational Biology, Scripps Research)

  • Kei Saotome

    (Department of Integrative Structural and Computational Biology, Scripps Research
    Howard Hughes Medical Institute, Department of Neuroscience, Dorris Neuroscience Center, Scripps Research
    Regeneron Pharmaceuticals)

  • Che Chun Alex Tsui

    (Department of Integrative Structural and Computational Biology, Scripps Research
    University of Oxford)

  • Wen-Hsin Lee

    (Department of Integrative Structural and Computational Biology, Scripps Research)

  • Mark S. P. Sansom

    (University of Oxford)

  • Swetha E. Murthy

    (Howard Hughes Medical Institute, Department of Neuroscience, Dorris Neuroscience Center, Scripps Research
    Oregon Health and Science University)

  • Ardem Patapoutian

    (Howard Hughes Medical Institute, Department of Neuroscience, Dorris Neuroscience Center, Scripps Research)

  • Andrew B. Ward

    (Department of Integrative Structural and Computational Biology, Scripps Research)

Abstract

Flycatcher1 (FLYC1), a MscS homolog, has recently been identified as a candidate mechanosensitive (MS) ion channel involved in Venus flytrap prey recognition. FLYC1 is a larger protein and its sequence diverges from previously studied MscS homologs, suggesting it has unique structural features that contribute to its function. Here, we characterize FLYC1 by cryo-electron microscopy, molecular dynamics simulations, and electrophysiology. Akin to bacterial MscS and plant MSL1 channels, we find that FLYC1 central core includes side portals in the cytoplasmic cage that regulate ion preference and conduction, by identifying critical residues that modulate channel conductance. Topologically unique cytoplasmic flanking regions can adopt ‘up’ or ‘down’ conformations, making the channel asymmetric. Disruption of an up conformation-specific interaction severely delays channel deactivation by 40-fold likely due to stabilization of the channel open state. Our results illustrate novel structural features and likely conformational transitions that regulate mechano-gating of FLYC1.

Suggested Citation

  • Sebastian Jojoa-Cruz & Kei Saotome & Che Chun Alex Tsui & Wen-Hsin Lee & Mark S. P. Sansom & Swetha E. Murthy & Ardem Patapoutian & Andrew B. Ward, 2022. "Structural insights into the Venus flytrap mechanosensitive ion channel Flycatcher1," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28511-5
    DOI: 10.1038/s41467-022-28511-5
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    References listed on IDEAS

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    1. C. D. Cox & T. Nomura & C. S. Ziegler & A. K. Campbell & K. T. Wann & B. Martinac, 2013. "Selectivity mechanism of the mechanosensitive channel MscS revealed by probing channel subconducting states," Nature Communications, Nature, vol. 4(1), pages 1-11, October.
    2. Zengqin Deng & Grigory Maksaev & Angela M. Schlegel & Jingying Zhang & Michael Rau & James A. J. Fitzpatrick & Elizabeth S. Haswell & Peng Yuan, 2020. "Structural mechanism for gating of a eukaryotic mechanosensitive channel of small conductance," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    3. Viktor Lukacs & Jayanti Mathur & Rong Mao & Pinar Bayrak-Toydemir & Melinda Procter & Stuart M. Cahalan & Helen J. Kim & Michael Bandell & Nicola Longo & Ronald W. Day & David A. Stevenson & Ardem Pat, 2015. "Impaired PIEZO1 function in patients with a novel autosomal recessive congenital lymphatic dysplasia," Nature Communications, Nature, vol. 6(1), pages 1-7, November.
    4. Yixiao Zhang & Csaba Daday & Ruo-Xu Gu & Charles D. Cox & Boris Martinac & Bert L. Groot & Thomas Walz, 2021. "Visualization of the mechanosensitive ion channel MscS under membrane tension," Nature, Nature, vol. 590(7846), pages 509-514, February.
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