Ultrafast structural changes within a photosynthetic reaction centre

Robert Dods^#¹, Petra Båth^#¹, Dmitry Morozov², Viktor Ahlberg Gagnér¹, David Arnlund¹, Hoi Ling Luk², Joachim Kübel¹, Michał Maj¹, Adams Vallejos¹, Cecilia Wickstrand¹, Robert Bosman¹, Kenneth R Beyerlein³, Garrett Nelson⁴, Mengning Liang⁵, Despina Milathianaki⁵, Joseph Robinson⁵, Rajiv Harimoorthy¹, Peter Berntsen^{1

6}, Erik Malmerberg⁷, Linda Johansson^{1

8}, Rebecka Andersson¹, Sergio Carbajo⁵, Elin Claesson¹, Chelsie E Conrad⁹, Peter Dahl¹, Greger Hammarin¹, Mark S Hunter⁵, Chufeng Li⁴, Stella Lisova⁴, Antoine Royant^{10

11}, Cecilia Safari¹, Amit Sharma¹, Garth J Williams⁵, Oleksandr Yefanov³, Sebastian Westenhoff¹, Jan Davidsson¹², Daniel P DePonte⁵, Sébastien Boutet⁵, Anton Barty³, Gergely Katona¹, Gerrit Groenhof², Gisela Brändén¹, Richard Neutze¹³

Affiliations

¹ Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden.
² Nanoscience Center and Department of Chemistry, University of Jyväskylä, Jyväskylä, Finland.
³ Centre for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron DESY, Hamburg, Germany.
⁴ Department of Physics, Arizona State University, Tempe, AZ, USA.
⁵ Linac Coherent Light Source, Stanford Linear Accelerator Centre (SLAC), National Accelerator Laboratory, Menlo Park, CA, USA.
⁶ Australian Research Council Centre of Excellence in Advanced Molecular Imaging, La Trobe Institute for Molecular Science, La Trobe University, Melbourne, Victoria, Australia.
⁷ Molecular Biophysics and Integrated Bioimaging, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
⁸ Bridge Institute, USC Michelson Center for Convergent Biosciences, University of Southern California, Los Angeles, CA, USA.
⁹ Department of Chemistry and Biochemistry, Arizona State University, Tempe, AZ, USA.
¹⁰ Institut de Biologie Structurale (IBS), Université Grenoble Alpes, CEA, CNRS, Grenoble, France.
¹¹ European Synchrotron Radiation Facility, Grenoble, France.
¹² Ångström Laboratory, Department of Chemistry, Uppsala University, Uppsala, Sweden.
¹³ Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden. richard.neutze@gu.se.

^# Contributed equally.

PMID: 33268896
DOI: 10.1038/s41586-020-3000-7

Ultrafast structural changes within a photosynthetic reaction centre

Robert Dods et al. Nature. 2021 Jan.

. 2021 Jan;589(7841):310-314.

doi: 10.1038/s41586-020-3000-7. Epub 2020 Dec 2.

Authors

Affiliations

¹ Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden.
² Nanoscience Center and Department of Chemistry, University of Jyväskylä, Jyväskylä, Finland.
³ Centre for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron DESY, Hamburg, Germany.
⁴ Department of Physics, Arizona State University, Tempe, AZ, USA.
⁵ Linac Coherent Light Source, Stanford Linear Accelerator Centre (SLAC), National Accelerator Laboratory, Menlo Park, CA, USA.
⁶ Australian Research Council Centre of Excellence in Advanced Molecular Imaging, La Trobe Institute for Molecular Science, La Trobe University, Melbourne, Victoria, Australia.
⁷ Molecular Biophysics and Integrated Bioimaging, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
⁸ Bridge Institute, USC Michelson Center for Convergent Biosciences, University of Southern California, Los Angeles, CA, USA.
⁹ Department of Chemistry and Biochemistry, Arizona State University, Tempe, AZ, USA.
¹⁰ Institut de Biologie Structurale (IBS), Université Grenoble Alpes, CEA, CNRS, Grenoble, France.
¹¹ European Synchrotron Radiation Facility, Grenoble, France.
¹² Ångström Laboratory, Department of Chemistry, Uppsala University, Uppsala, Sweden.
¹³ Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden. richard.neutze@gu.se.

^# Contributed equally.

PMID: 33268896
DOI: 10.1038/s41586-020-3000-7

Abstract

Photosynthetic reaction centres harvest the energy content of sunlight by transporting electrons across an energy-transducing biological membrane. Here we use time-resolved serial femtosecond crystallography¹ using an X-ray free-electron laser² 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.

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References

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1. Breton, J., Martin, J. L., Migus, A., Antonetti, A. & Orszag, A. Femtosecond spectroscopy of excitation energy transfer and initial charge separation in the reaction center of the photosynthetic bacterium Rhodopseudomonas viridis. Proc. Natl Acad. Sci. USA 83, 5121–5125 (1986). - PubMed - PMC
1. Chan, C. K., DiMagno, T. J., Chen, L. X., Norris, J. R. & Fleming, G. R. Mechanism of the initial charge separation in bacterial photosynthetic reaction centers. Proc. Natl Acad. Sci. USA 88, 11202–11206 (1991). - PubMed - PMC

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Ultrafast structural changes within a photosynthetic reaction centre

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Ultrafast structural changes within a photosynthetic reaction centre

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