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Femtosecond-to-millisecond structural changes in a light-driven sodium pump

Author

Listed:
  • Petr Skopintsev

    (Paul Scherrer Institut)

  • David Ehrenberg

    (Freie Universität Berlin)

  • Tobias Weinert

    (Paul Scherrer Institut)

  • Daniel James

    (Paul Scherrer Institut)

  • Rajiv K. Kar

    (The Hebrew University of Jerusalem)

  • Philip J. M. Johnson

    (Paul Scherrer Institut)

  • Dmitry Ozerov

    (Science IT, Paul Scherrer Institut)

  • Antonia Furrer

    (Paul Scherrer Institut)

  • Isabelle Martiel

    (Paul Scherrer Institut)

  • Florian Dworkowski

    (Paul Scherrer Institut)

  • Karol Nass

    (Paul Scherrer Institut
    Paul Scherrer Institut)

  • Gregor Knopp

    (Paul Scherrer Institut)

  • Claudio Cirelli

    (Paul Scherrer Institut)

  • Christopher Arrell

    (Paul Scherrer Institut)

  • Dardan Gashi

    (Paul Scherrer Institut
    Paul Scherrer Institut)

  • Sandra Mous

    (ETH Zürich)

  • Maximilian Wranik

    (Paul Scherrer Institut)

  • Thomas Gruhl

    (Paul Scherrer Institut)

  • Demet Kekilli

    (Paul Scherrer Institut)

  • Steffen Brünle

    (Paul Scherrer Institut)

  • Xavier Deupi

    (Paul Scherrer Institut
    Paul Scherrer Institut)

  • Gebhard F. X. Schertler

    (Paul Scherrer Institut
    ETH Zürich)

  • Roger M. Benoit

    (Paul Scherrer Institut
    Paul Scherrer Institut)

  • Valerie Panneels

    (Paul Scherrer Institut)

  • Przemyslaw Nogly

    (ETH Zürich)

  • Igor Schapiro

    (The Hebrew University of Jerusalem)

  • Christopher Milne

    (Paul Scherrer Institut)

  • Joachim Heberle

    (Freie Universität Berlin)

  • Jörg Standfuss

    (Paul Scherrer Institut)

Abstract

Light-driven sodium pumps actively transport small cations across cellular membranes1. These pumps are used by microorganisms to convert light into membrane potential and have become useful optogenetic tools with applications in neuroscience. Although the resting state structures of the prototypical sodium pump Krokinobacter eikastus rhodopsin 2 (KR2) have been solved2,3, it is unclear how structural alterations over time allow sodium to be translocated against a concentration gradient. Here, using the Swiss X-ray Free Electron Laser4, we have collected serial crystallographic data at ten pump–probe delays from femtoseconds to milliseconds. High-resolution structural snapshots throughout the KR2 photocycle show how retinal isomerization is completed on the femtosecond timescale and changes the local structure of the binding pocket in the early nanoseconds. Subsequent rearrangements and deprotonation of the retinal Schiff base open an electrostatic gate in microseconds. Structural and spectroscopic data, in combination with quantum chemical calculations, indicate that a sodium ion binds transiently close to the retinal within one millisecond. In the last structural intermediate, at 20 milliseconds after activation, we identified a potential second sodium-binding site close to the extracellular exit. These results provide direct molecular insight into the dynamics of active cation transport across biological membranes.

Suggested Citation

  • Petr Skopintsev & David Ehrenberg & Tobias Weinert & Daniel James & Rajiv K. Kar & Philip J. M. Johnson & Dmitry Ozerov & Antonia Furrer & Isabelle Martiel & Florian Dworkowski & Karol Nass & Gregor K, 2020. "Femtosecond-to-millisecond structural changes in a light-driven sodium pump," Nature, Nature, vol. 583(7815), pages 314-318, July.
  • Handle: RePEc:nat:nature:v:583:y:2020:i:7815:d:10.1038_s41586-020-2307-8
    DOI: 10.1038/s41586-020-2307-8
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    Cited by:

    1. Basudev Maity & Mitsuo Shoji & Fangjia Luo & Takanori Nakane & Satoshi Abe & Shigeki Owada & Jungmin Kang & Kensuke Tono & Rie Tanaka & Thuc Toan Pham & Mariko Kojima & Yuki Hishikawa & Junko Tanaka &, 2024. "Real-time observation of a metal complex-driven reaction intermediate using a porous protein crystal and serial femtosecond crystallography," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. E. Podoliak & G. H. U. Lamm & E. Marin & A. V. Schellbach & D. A. Fedotov & A. Stetsenko & M. Asido & N. Maliar & G. Bourenkov & T. Balandin & C. Baeken & R. Astashkin & T. R. Schneider & A. Bateman &, 2024. "A subgroup of light-driven sodium pumps with an additional Schiff base counterion," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Maximilian Wranik & Michal W. Kepa & Emma V. Beale & Daniel James & Quentin Bertrand & Tobias Weinert & Antonia Furrer & Hannah Glover & Dardan Gashi & Melissa Carrillo & Yasushi Kondo & Robin T. Stip, 2023. "A multi-reservoir extruder for time-resolved serial protein crystallography and compound screening at X-ray free-electron lasers," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    4. Maximilian Wranik & Tobias Weinert & Chavdar Slavov & Tiziana Masini & Antonia Furrer & Natacha Gaillard & Dario Gioia & Marco Ferrarotti & Daniel James & Hannah Glover & Melissa Carrillo & Demet Keki, 2023. "Watching the release of a photopharmacological drug from tubulin using time-resolved serial crystallography," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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