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Title: Ultrafast structural changes within a photosynthetic reaction centre

Abstract

Photosynthetic reaction centres harvest the energy content of sunlight by transporting electrons across an energy-transducing biological membrane. In this study we use time-resolved serial femtosecond crystallography using an X-ray free-electron laser to observe light-induced structural changes in the photosynthetic reaction centre of Blastochloris viridis on a timescale of picoseconds. Structural perturbations first occur at the special pair of chlorophyll molecules of the photosynthetic reaction centre that are photo-oxidized by light. Electron transfer to the menaquinone acceptor on the opposite side of the membrane induces a movement of this cofactor together with lower amplitude protein rearrangements. These observations reveal how proteins use conformational dynamics to stabilize the charge-separation steps of electron-transfer reactions.

Authors:
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  1. Univ. of Gothenburg (Sweden)
  2. Univ. of Jyvaskyla (Finland)
  3. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany). Center for Free-Electron Laser Science
  4. Arizona State Univ., Tempe, AZ (United States)
  5. SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
  6. Univ. of Gothenburg (Sweden); La Trobe Univ., Melbourne, VIC (Australia)
  7. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  8. Univ. of Gothenburg (Sweden); Univ. of Southern California, Los Angeles, CA (United States)
  9. Univ. Grenoble Alpes (France); European Synchrotron Radiation Facility (ESRF), Grenoble (France)
  10. Uppsala Univ. (Sweden)
Publication Date:
Research Org.:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); Japan Synchrotron Radiation Research Institute (JASRI); European Commission (EC); Swedish Research Council (SRC); Swedish Foundation for Strategic Research; Knut and Alice Wallenberg Foundation; Academy of Finland
OSTI Identifier:
1768403
Grant/Contract Number:  
AC02-76SF00515; P41GM103393; 2018B8068; 789030; 2015-00560; 349-2011-6485; 2017-06734; SRL10-0036; ID17-0060; KAW 2012.0284; KAW 2012.0275; KAW 2014.0275; 290677; 304455; H2020-INFRAEDI-02-2018-823830; H2020-EINFRA-2015-1-675728
Resource Type:
Accepted Manuscript
Journal Name:
Nature (London)
Additional Journal Information:
Journal Name: Nature (London); Journal Volume: 589; Journal Issue: 7841; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Dods, Robert, Båth, Petra, Morozov, Dmitry, Gagnér, Viktor Ahlberg, Arnlund, David, Luk, Hoi Ling, Kübel, Joachim, Maj, Michał, Vallejos, Adams, Wickstrand, Cecilia, Bosman, Robert, Beyerlein, Kenneth R., Nelson, Garrett, Liang, Mengning, Milathianaki, Despina, Robinson, Joseph, Harimoorthy, Rajiv, Berntsen, Peter, Malmerberg, Erik, Johansson, Linda, Andersson, Rebecka, Carbajo, Sergio, Claesson, Elin, Conrad, Chelsie E., Dahl, Peter, Hammarin, Greger, Hunter, Mark S., Li, Chufeng, Lisova, Stella, Royant, Antoine, Safari, Cecilia, Sharma, Amit, Williams, Garth J., Yefanov, Oleksandr, Westenhoff, Sebastian, Davidsson, Jan, DePonte, Daniel P., Boutet, Sébastien, Barty, Anton, Katona, Gergely, Groenhof, Gerrit, Brändén, Gisela, and Neutze, Richard. Ultrafast structural changes within a photosynthetic reaction centre. United States: N. p., 2020. Web. doi:10.1038/s41586-020-3000-7.
Dods, Robert, Båth, Petra, Morozov, Dmitry, Gagnér, Viktor Ahlberg, Arnlund, David, Luk, Hoi Ling, Kübel, Joachim, Maj, Michał, Vallejos, Adams, Wickstrand, Cecilia, Bosman, Robert, Beyerlein, Kenneth R., Nelson, Garrett, Liang, Mengning, Milathianaki, Despina, Robinson, Joseph, Harimoorthy, Rajiv, Berntsen, Peter, Malmerberg, Erik, Johansson, Linda, Andersson, Rebecka, Carbajo, Sergio, Claesson, Elin, Conrad, Chelsie E., Dahl, Peter, Hammarin, Greger, Hunter, Mark S., Li, Chufeng, Lisova, Stella, Royant, Antoine, Safari, Cecilia, Sharma, Amit, Williams, Garth J., Yefanov, Oleksandr, Westenhoff, Sebastian, Davidsson, Jan, DePonte, Daniel P., Boutet, Sébastien, Barty, Anton, Katona, Gergely, Groenhof, Gerrit, Brändén, Gisela, & Neutze, Richard. Ultrafast structural changes within a photosynthetic reaction centre. United States. https://doi.org/10.1038/s41586-020-3000-7
Dods, Robert, Båth, Petra, Morozov, Dmitry, Gagnér, Viktor Ahlberg, Arnlund, David, Luk, Hoi Ling, Kübel, Joachim, Maj, Michał, Vallejos, Adams, Wickstrand, Cecilia, Bosman, Robert, Beyerlein, Kenneth R., Nelson, Garrett, Liang, Mengning, Milathianaki, Despina, Robinson, Joseph, Harimoorthy, Rajiv, Berntsen, Peter, Malmerberg, Erik, Johansson, Linda, Andersson, Rebecka, Carbajo, Sergio, Claesson, Elin, Conrad, Chelsie E., Dahl, Peter, Hammarin, Greger, Hunter, Mark S., Li, Chufeng, Lisova, Stella, Royant, Antoine, Safari, Cecilia, Sharma, Amit, Williams, Garth J., Yefanov, Oleksandr, Westenhoff, Sebastian, Davidsson, Jan, DePonte, Daniel P., Boutet, Sébastien, Barty, Anton, Katona, Gergely, Groenhof, Gerrit, Brändén, Gisela, and Neutze, Richard. Wed . "Ultrafast structural changes within a photosynthetic reaction centre". United States. https://doi.org/10.1038/s41586-020-3000-7. https://www.osti.gov/servlets/purl/1768403.
@article{osti_1768403,
title = {Ultrafast structural changes within a photosynthetic reaction centre},
author = {Dods, Robert and Båth, Petra and Morozov, Dmitry and Gagnér, Viktor Ahlberg and Arnlund, David and Luk, Hoi Ling and Kübel, Joachim and Maj, Michał and Vallejos, Adams and Wickstrand, Cecilia and Bosman, Robert and Beyerlein, Kenneth R. and Nelson, Garrett and Liang, Mengning and Milathianaki, Despina and Robinson, Joseph and Harimoorthy, Rajiv and Berntsen, Peter and Malmerberg, Erik and Johansson, Linda and Andersson, Rebecka and Carbajo, Sergio and Claesson, Elin and Conrad, Chelsie E. and Dahl, Peter and Hammarin, Greger and Hunter, Mark S. and Li, Chufeng and Lisova, Stella and Royant, Antoine and Safari, Cecilia and Sharma, Amit and Williams, Garth J. and Yefanov, Oleksandr and Westenhoff, Sebastian and Davidsson, Jan and DePonte, Daniel P. and Boutet, Sébastien and Barty, Anton and Katona, Gergely and Groenhof, Gerrit and Brändén, Gisela and Neutze, Richard},
abstractNote = {Photosynthetic reaction centres harvest the energy content of sunlight by transporting electrons across an energy-transducing biological membrane. In this study we use time-resolved serial femtosecond crystallography using an X-ray free-electron laser to observe light-induced structural changes in the photosynthetic reaction centre of Blastochloris viridis on a timescale of picoseconds. Structural perturbations first occur at the special pair of chlorophyll molecules of the photosynthetic reaction centre that are photo-oxidized by light. Electron transfer to the menaquinone acceptor on the opposite side of the membrane induces a movement of this cofactor together with lower amplitude protein rearrangements. These observations reveal how proteins use conformational dynamics to stabilize the charge-separation steps of electron-transfer reactions.},
doi = {10.1038/s41586-020-3000-7},
journal = {Nature (London)},
number = 7841,
volume = 589,
place = {United States},
year = {Wed Dec 02 00:00:00 EST 2020},
month = {Wed Dec 02 00:00:00 EST 2020}
}

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Works referencing / citing this record:

Ultrafast structural response to charge redistribution within a photosinthetic reaction centre
dataset, January 2020

  • Dods, Robert; Båth, Petra
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BioExcel-2 deliverable D3.6 – Pre-Exascale showcase calculation and Use Case Final Report
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BioExcel-2 deliverable D3.6 – Pre-Exascale showcase calculation and Use Case Final Report
text, January 2022