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

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 Knopp, Claudio Cirelli, Christopher Arrell, Dardan Gashi, Sandra Mous, Maximilian Wranik, Thomas Gruhl, Demet Kekilli, Steffen Brünle, Xavier Deupi, Gebhard F. X. Schertler, Roger M. Benoit, Valerie Panneels, Przemyslaw Nogly, Igor Schapiro, Christopher Milne, Joachim Heberle and Jörg Standfuss ()
Additional contact information
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
Gregor Knopp: Paul Scherrer Institut
Claudio Cirelli: Paul Scherrer Institut
Christopher Arrell: Paul Scherrer Institut
Dardan Gashi: 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
Gebhard F. X. Schertler: Paul Scherrer Institut
Roger M. Benoit: 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

Nature, 2020, vol. 583, issue 7815, 314-318

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41586-020-2307-8

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