The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser

  1. Elin Claesson
  2. Weixiao Yuan Wahlgren
  3. Heikki Takala
  4. Suraj Pandey
  5. Leticia Castillon
  6. Valentyna Kuznetsova
  7. Léocadie Henry
  8. Matthijs Panman
  9. Melissa Carrillo
  10. Joachim Kübel
  11. Rahul Nanekar
  12. Linnéa Isaksson
  13. Amke Nimmrich
  14. Andrea Cellini
  15. Dmitry Morozov
  16. Michał Maj
  17. Moona Kurttila
  18. Robert Bosman
  19. Eriko Nango
  20. Rie Tanaka
  21. Tomoyuki Tanaka
  22. Luo Fangjia
  23. So Iwata
  24. Shigeki Owada
  25. Keith Moffat
  26. Gerrit Groenhof
  27. Emina A. Stojković
  28. Janne A. Ihalainen
  29. Marius Schmidt  Is a corresponding author
  30. Sebastian Westenhoff  Is a corresponding author
  1. University of Gothenburg, Sweden
  2. University of Jyvaskyla, Finland
  3. University of Wisconsin-Milwaukee, United States
  4. Northeastern Illinois University, United States
  5. Kyoto University, Japan
  6. University of Chicago, United States

Abstract

Phytochrome proteins control the growth, reproduction, and photosynthesis of plants, fungi, and bacteria. Light is detected by a bilin cofactor, but it remains elusive how this leads to activation of the protein through structural changes. We present serial femtosecond X-ray crystallographic data of the chromophore-binding domains of a bacterial phytochrome at delay times of 1 ps and 10 ps after photoexcitation. The data reveal a twist of the D-ring, which leads to partial detachment of the chromophore from the protein. Unexpectedly, the conserved so-called pyrrole water is photodissociated from the chromophore, concomitant with movement of the A-ring and a key signalling aspartate. The changes are wired together by ultrafast backbone and water movements around the chromophore, channeling them into signal transduction towards the output domains. We suggest that the observed collective changes are important for the phytochrome photoresponse, explaining the earliest steps of how plants, fungi and bacteria sense red light.

Data availability

Crystallography data have been submitted to protein data bank (PDB)dark:ID: D_1292104678 and PDB ID: 6T3L1ps:ID: D_1292104679 and PDB ID: 6T3URaw diffraction images are in the process of being uploaded to CXIDB

The following data sets were generated

Article and author information

Author details

  1. Elin Claesson

    Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  2. Weixiao Yuan Wahlgren

    Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  3. Heikki Takala

    Department of Biological and Environmental Sciences, University of Jyvaskyla, Jyvaskyla, Finland
    Competing interests
    The authors declare that no competing interests exist.
  4. Suraj Pandey

    University of Wisconsin-Milwauke, University of Wisconsin-Milwaukee, Wisconsin, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Leticia Castillon

    Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  6. Valentyna Kuznetsova

    Department of Biological and Environmental Sciences, University of Jyvaskyla, Jyvaskyla, Finland
    Competing interests
    The authors declare that no competing interests exist.
  7. Léocadie Henry

    Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  8. Matthijs Panman

    Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3853-123X
  9. Melissa Carrillo

    Department of Biology, Northeastern Illinois University, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Joachim Kübel

    Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  11. Rahul Nanekar

    Department of Biological and Environmental Sciences, University of Jyvaskyla, Jyvaskyla, Finland
    Competing interests
    The authors declare that no competing interests exist.
  12. Linnéa Isaksson

    Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  13. Amke Nimmrich

    Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  14. Andrea Cellini

    Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  15. Dmitry Morozov

    Department of Chemistry, University of Jyvaskyla, Jyvaskyla, Finland
    Competing interests
    The authors declare that no competing interests exist.
  16. Michał Maj

    Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  17. Moona Kurttila

    Department of Biological and Environmental Sciences, University of Jyvaskyla, Jyvaskyla, Finland
    Competing interests
    The authors declare that no competing interests exist.
  18. Robert Bosman

    Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  19. Eriko Nango

    Department of Cell Biology, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  20. Rie Tanaka

    Department of Cell Biology, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  21. Tomoyuki Tanaka

    Department of Cell Biology, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  22. Luo Fangjia

    Department of Cell Biology, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  23. So Iwata

    Department of Cell Biology, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  24. Shigeki Owada

    RIKEN SPring-8 Center, Kyoto University, Hyogo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  25. Keith Moffat

    Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  26. Gerrit Groenhof

    Department of Chemistry, University of Jyvaskyla, Jyvaskyla, Finland
    Competing interests
    The authors declare that no competing interests exist.
  27. Emina A. Stojković

    Department of Biology, Northeastern Illinois University, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  28. Janne A. Ihalainen

    Department of Biological and Environmental Sciences, University of Jyvaskyla, Jyvaskyla, Finland
    Competing interests
    The authors declare that no competing interests exist.
  29. Marius Schmidt

    University of Wisconsin-Milwauke, University of Wisconsin-Milwaukee, Wisconsin, United States
    For correspondence
    smarius@uwm.edu
    Competing interests
    The authors declare that no competing interests exist.
  30. Sebastian Westenhoff

    Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
    For correspondence
    sebastian.westenhoff.2@gu.se
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6961-8015

Funding

European Research Council (279944)

  • Sebastian Westenhoff

Academy of Finland (285461)

  • Sebastian Westenhoff

Academy of Finland (296135)

  • Sebastian Westenhoff

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Werner Kühlbrandt, Max Planck Institute of Biophysics, Germany

Publication history

  1. Received: November 11, 2019
  2. Accepted: March 13, 2020
  3. Accepted Manuscript published: March 31, 2020 (version 1)
  4. Version of Record published: April 17, 2020 (version 2)

Copyright

© 2020, Claesson et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Elin Claesson
  2. Weixiao Yuan Wahlgren
  3. Heikki Takala
  4. Suraj Pandey
  5. Leticia Castillon
  6. Valentyna Kuznetsova
  7. Léocadie Henry
  8. Matthijs Panman
  9. Melissa Carrillo
  10. Joachim Kübel
  11. Rahul Nanekar
  12. Linnéa Isaksson
  13. Amke Nimmrich
  14. Andrea Cellini
  15. Dmitry Morozov
  16. Michał Maj
  17. Moona Kurttila
  18. Robert Bosman
  19. Eriko Nango
  20. Rie Tanaka
  21. Tomoyuki Tanaka
  22. Luo Fangjia
  23. So Iwata
  24. Shigeki Owada
  25. Keith Moffat
  26. Gerrit Groenhof
  27. Emina A. Stojković
  28. Janne A. Ihalainen
  29. Marius Schmidt
  30. Sebastian Westenhoff
(2020)
The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser
eLife 9:e53514.
https://doi.org/10.7554/eLife.53514

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