IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-58263-x.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-58263-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-025-58263-x?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. Susannah Holmes & Henry J. Kirkwood & Richard Bean & Klaus Giewekemeyer & Andrew V. Martin & Marjan Hadian-Jazi & Max O. Wiedorn & Dominik Oberthür & Hugh Marman & Luigi Adriano & Nasser Al-Qudami & S, 2022. "Megahertz pulse trains enable multi-hit serial femtosecond crystallography experiments at X-ray free electron lasers," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Quentin Bertrand & Przemyslaw Nogly & Eriko Nango & Demet Kekilli & Georgii Khusainov & Antonia Furrer & Daniel James & Florian Dworkowski & Petr Skopintsev & Sandra Mous & Isabelle Martiel & Per Börj, 2024. "Structural effects of high laser power densities on an early bacteriorhodopsin photocycle intermediate," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    4. 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.
    5. Gábor Bortel & Miklós Tegze & Marcin Sikorski & Richard Bean & Johan Bielecki & Chan Kim & Jayanath C. P. Koliyadu & Faisal H. M. Koua & Marco Ramilli & Adam Round & Tokushi Sato & Dmitrii Zabelskii &, 2024. "3D atomic structure from a single X-ray free electron laser pulse," Nature Communications, Nature, vol. 15(1), pages 1-7, December.
    6. Mengke Li & Hongzhi Tang & Rui Qing & Yanze Wang & Jiongqin Liu & Rui Wang & Shan Lyu & Lina Ma & Ping Xu & Shuguang Zhang & Fei Tao, 2024. "Design of a water-soluble transmembrane receptor kinase with intact molecular function by QTY code," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Mario Reiser & Anita Girelli & Anastasia Ragulskaya & Sudipta Das & Sharon Berkowicz & Maddalena Bin & Marjorie Ladd-Parada & Mariia Filianina & Hanna-Friederike Poggemann & Nafisa Begam & Mohammad Sa, 2022. "Resolving molecular diffusion and aggregation of antibody proteins with megahertz X-ray free-electron laser pulses," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    8. Alma P. Perrino & Atsushi Miyagi & Simon Scheuring, 2021. "Single molecule kinetics of bacteriorhodopsin by HS-AFM," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    9. Stephan Kuschel & Phay J. Ho & Andre Al Haddad & Felix F. Zimmermann & Leonie Flueckiger & Matthew R. Ware & Joseph Duris & James P. MacArthur & Alberto Lutman & Ming-Fu Lin & Xiang Li & Kazutaka Naka, 2025. "Non-linear enhancement of ultrafast X-ray diffraction through transient resonances," Nature Communications, Nature, vol. 16(1), pages 1-8, December.
    10. Jiaqi Zhou & Xitao Yu & Sizuo Luo & Xiaorui Xue & Shaokui Jia & Xinyu Zhang & Yongtao Zhao & Xintai Hao & Lanhai He & Chuncheng Wang & Dajun Ding & Xueguang Ren, 2022. "Triple ionization and fragmentation of benzene trimers following ultrafast intermolecular Coulombic decay," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    11. Jincong Pang & Haodi Wu & Hao Li & Tong Jin & Jiang Tang & Guangda Niu, 2024. "Reconfigurable perovskite X-ray detector for intelligent imaging," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    12. Natasha L. George & Benjamin J. Orlando, 2023. "Architecture of a complete Bce-type antimicrobial peptide resistance module," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    13. Lin Zhang & Beibei Sun & Fei Shu & Ying Huang, 2022. "Comparing paper level classifications across different methods and systems: an investigation of Nature publications," Scientometrics, Springer;Akadémiai Kiadó, vol. 127(12), pages 7633-7651, December.
    14. Anna Wach & Robert Bericat-Vadell & Camila Bacellar & Claudio Cirelli & Philip J. M. Johnson & Rebeca G. Castillo & Vitor R. Silveira & Peter Broqvist & Jolla Kullgren & Alexey Maximenko & Tomasz Sobo, 2025. "The dynamics of plasmon-induced hot carrier creation in colloidal gold," Nature Communications, Nature, vol. 16(1), pages 1-12, December.
    15. Da Liu & Yichu Zheng & Xin Yuan Sui & Xue Feng Wu & Can Zou & Yu Peng & Xinyi Liu & Miaoyu Lin & Zhanpeng Wei & Hang Zhou & Ye-Feng Yao & Sheng Dai & Haiyang Yuan & Hua Gui Yang & Shuang Yang & Yu Hou, 2024. "Universal growth of perovskite thin monocrystals from high solute flux for sensitive self-driven X-ray detection," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    16. repec:plo:pcbi00:1002878 is not listed on IDEAS
    17. Kaihua Zhang & Hao Wu & Nicholas Hoppe & Aashish Manglik & Yifan Cheng, 2022. "Fusion protein strategies for cryo-EM study of G protein-coupled receptors," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    18. Volha U. Chukhutsina & James M. Baxter & Alisia Fadini & Rhodri M. Morgan & Matthew A. Pope & Karim Maghlaoui & Christian M. Orr & Armin Wagner & Jasper J. Thor, 2022. "Light activation of Orange Carotenoid Protein reveals bicycle-pedal single-bond isomerization," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    19. Elizaveta Lyapina & Egor Marin & Anastasiia Gusach & Philipp Orekhov & Andrey Gerasimov & Aleksandra Luginina & Daniil Vakhrameev & Margarita Ergasheva & Margarita Kovaleva & Georgii Khusainov & Polin, 2022. "Structural basis for receptor selectivity and inverse agonism in S1P5 receptors," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    20. Aljoscha Rörig & Sang-Kil Son & Tommaso Mazza & Philipp Schmidt & Thomas M. Baumann & Benjamin Erk & Markus Ilchen & Joakim Laksman & Valerija Music & Shashank Pathak & Daniel E. Rivas & Daniel Rolles, 2023. "Multiple-core-hole resonance spectroscopy with ultraintense X-ray pulses," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    21. Michael W. Martynowycz & Anna Shiriaeva & Max T. B. Clabbers & William J. Nicolas & Sara J. Weaver & Johan Hattne & Tamir Gonen, 2023. "A robust approach for MicroED sample preparation of lipidic cubic phase embedded membrane protein crystals," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-58263-x. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.