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Structural basis for the prolonged photocycle of sensory rhodopsin II revealed by serial synchrotron crystallography

Author

Listed:
  • Robert Bosman

    (University of Gothenburg)

  • Giorgia Ortolani

    (University of Gothenburg)

  • Swagatha Ghosh

    (University of Gothenburg)

  • Daniel James

    (Forschungsstrasse 111)

  • Per Norder

    (University of Gothenburg)

  • Greger Hammarin

    (University of Gothenburg)

  • Tinna Björg Úlfarsdóttir

    (University of Gothenburg)

  • Lucija Ostojić

    (University of Gothenburg)

  • Tobias Weinert

    (Forschungsstrasse 111)

  • Florian Dworkowski

    (Forschungsstrasse 111)

  • Takashi Tomizaki

    (Forschungsstrasse 111)

  • Jörg Standfuss

    (Forschungsstrasse 111)

  • Gisela Brändén

    (University of Gothenburg)

  • Richard Neutze

    (University of Gothenburg)

Abstract

Microbial rhodopsins form a diverse family of light-sensitive seven-transmembrane helix retinal proteins that function as active proton or ion pumps, passive light-gated ion channels, and photosensors. To understand how light-sensing in archaea is initiated by sensory rhodopsins, we perform serial synchrotron X-ray crystallography (SSX) studies of light induced conformational changes in sensory rhodopsin II (NpSRII) from the archaea Natronomonas pharaonis, both collecting time-resolved SSX data and collecting SSX data during continuous illumination. Comparing light-induced electron density changes in NpSRII with those reported for bacteriorhodopsin (bR) reveals several common light-induced structural perturbations. Unlike bR, however, helix G of NpSRII does not unwind near the conserved lysine residue to which retinal is covalently bound and therefore transient water molecule binding sites do not arise immediately to the cytoplasmic side of retinal. These structural differences prolong the duration of the NpSRII photocycle relative to bR, allowing time for the light-initiated sensory signal to be amplified.

Suggested Citation

  • Robert Bosman & Giorgia Ortolani & Swagatha Ghosh & Daniel James & Per Norder & Greger Hammarin & Tinna Björg Úlfarsdóttir & Lucija Ostojić & Tobias Weinert & Florian Dworkowski & Takashi Tomizaki & J, 2025. "Structural basis for the prolonged photocycle of sensory rhodopsin II revealed by serial synchrotron crystallography," Nature Communications, Nature, vol. 16(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-58263-x
    DOI: 10.1038/s41467-025-58263-x
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    1. Rouslan Moukhametzianov & Johann P. Klare & Rouslan Efremov & Christian Baeken & Annika Göppner & Jörg Labahn & Martin Engelhard & Georg Büldt & Valentin I. Gordeliy, 2006. "Development of the signal in sensory rhodopsin and its transfer to the cognate transducer," Nature, Nature, vol. 440(7080), pages 115-119, March.
    2. Richard Neutze & Remco Wouts & David van der Spoel & Edgar Weckert & Janos Hajdu, 2000. "Potential for biomolecular imaging with femtosecond X-ray pulses," Nature, Nature, vol. 406(6797), pages 752-757, August.
    3. Uwe Weierstall & Daniel James & Chong Wang & Thomas A. White & Dingjie Wang & Wei Liu & John C. H. Spence & R. Bruce Doak & Garrett Nelson & Petra Fromme & Raimund Fromme & Ingo Grotjohann & Christoph, 2014. "Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography," Nature Communications, Nature, vol. 5(1), pages 1-6, May.
    4. Henry N. Chapman & Petra Fromme & Anton Barty & Thomas A. White & Richard A. Kirian & Andrew Aquila & Mark S. Hunter & Joachim Schulz & Daniel P. DePonte & Uwe Weierstall & R. Bruce Doak & Filipe R. N, 2011. "Femtosecond X-ray protein nanocrystallography," Nature, Nature, vol. 470(7332), pages 73-77, February.
    5. Valentin I. Gordeliy & Jörg Labahn & Rouslan Moukhametzianov & Rouslan Efremov & Joachim Granzin & Ramona Schlesinger & Georg Büldt & Tudor Savopol & Axel J. Scheidig & Johann P. Klare & Martin Engelh, 2002. "Molecular basis of transmembrane signalling by sensory rhodopsin II–transducer complex," Nature, Nature, vol. 419(6906), pages 484-487, October.
    6. Gabriela Nass Kovacs & Jacques-Philippe Colletier & Marie Luise Grünbein & Yang Yang & Till Stensitzki & Alexander Batyuk & Sergio Carbajo & R. Bruce Doak & David Ehrenberg & Lutz Foucar & Raphael Gas, 2019. "Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    7. Antoine Royant & Karl Edman & Thomas Ursby & Eva Pebay-Peyroula & Ehud M. Landau & Richard Neutze, 2000. "Helix deformation is coupled to vectorial proton transport in the photocycle of bacteriorhodopsin," Nature, Nature, vol. 406(6796), pages 645-648, August.
    8. Karl Edman & Peter Nollert & Antoine Royant & Hassan Belrhali & Eva Pebay-Peyroula & Janos Hajdu & Richard Neutze & Ehud M. Landau, 1999. "High-resolution X-ray structure of an early intermediate in the bacteriorhodopsin photocycle," Nature, Nature, vol. 401(6755), pages 822-826, October.
    9. Linda C. Johansson & David Arnlund & Gergely Katona & Thomas A. White & Anton Barty & Daniel P. DePonte & Robert L. Shoeman & Cecilia Wickstrand & Amit Sharma & Garth J. Williams & Andrew Aquila & Mic, 2013. "Structure of a photosynthetic reaction centre determined by serial femtosecond crystallography," Nature Communications, Nature, vol. 4(1), pages 1-7, December.
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