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Title: Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography

Abstract

Chromophores absorb light in photosensitive proteins and thereby initiate fundamental biological processes such as photosynthesis, vision and biofluorescence. An important goal in their understanding is the provision of detailed structural descriptions of the ultrafast photochemical events that they undergo, in particular of the excited states that connect chemistry to biological function. Here in this paper we report on the structures of two excited states in the reversibly photoswitchable fluorescent protein rsEGFP2. We populated the states through femtosecond illumination of rsEGFP2 in its non-fluorescent off state and observed their build-up (within less than one picosecond) and decay (on the several picosecond timescale). Using an X-ray free-electron laser, we performed picosecond time-resolved crystallography and show that the hydroxybenzylidene imidazolinone chromophore in one of the excited states assumes a near-canonical twisted configuration halfway between the trans and cis isomers. This is in line with excited-state quantum mechanics/molecular mechanics and classical molecular dynamics simulations. Our new understanding of the structure around the twisted chromophore enabled the design of a mutant that displays a twofold increase in its off-to-on photoswitching quantum yield.

Authors:
 [1]; ORCiD logo [2];  [1];  [1]; ORCiD logo [1];  [3];  [4];  [3];  [1];  [3];  [1];  [4];  [1];  [1];  [4];  [1];  [4];  [3]; ORCiD logo [5];  [3] more »;  [4];  [3];  [6];  [3];  [4];  [6];  [3];  [4];  [2];  [3];  [1]; ORCiD logo [7];  [6]; ORCiD logo [1];  [4];  [1]; ORCiD logo [1];  [4]; ORCiD logo [1] « less
+ Show Author Affiliations
  1. Univ. of Grenoble (France). Inst. de Biologie Structurale
  2. Univ. de Lille (France). Lab. de Spectrochimie Infrarouge et Raman
  3. SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
  4. Max-Planck-Inst. fur medizinische Forschung, Heidelberg (Germany)
  5. Max-Planck-Inst. fur biophysikalische Chemie, Gottingen (Germany)
  6. Univ. Paris-Sud, Orsay (France); Univ. Paris-Saclay, Orsay (France). Lab. de Chimie-Physique
  7. Univ. of Rennes, Rennes (France). Dept. of Physics
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); European Union (EU)
OSTI Identifier:
1426209
Grant/Contract Number:  
AC02-76SF00515
Resource Type:
Accepted Manuscript
Journal Name:
Nature Chemistry
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 1755-4330
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
77 NANOSCIENCE AND NANOTECHNOLOGY; 59 BASIC BIOLOGICAL SCIENCES; Nanocrystallography; Photobiology; Protein structure predictions

Citation Formats

Coquelle, Nicolas, Sliwa, Michel, Woodhouse, Joyce, Schirò, Giorgio, Adam, Virgile, Aquila, Andrew, Barends, Thomas R. M., Boutet, Sébastien, Byrdin, Martin, Carbajo, Sergio, De la Mora, Eugenio, Doak, R. Bruce, Feliks, Mikolaj, Fieschi, Franck, Foucar, Lutz, Guillon, Virginia, Hilpert, Mario, Hunter, Mark S., Jakobs, Stefan, Koglin, Jason E., Kovacsova, Gabriela, Lane, Thomas J., Lévy, Bernard, Liang, Mengning, Nass, Karol, Ridard, Jacqueline, Robinson, Joseph S., Roome, Christopher M., Ruckebusch, Cyril, Seaberg, Matthew, Thepaut, Michel, Cammarata, Marco, Demachy, Isabelle, Field, Martin, Shoeman, Robert L., Bourgeois, Dominique, Colletier, Jacques-Philippe, Schlichting, Ilme, and Weik, Martin. Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography. United States: N. p., 2017. Web. doi:10.1038/nchem.2853.
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Coquelle, Nicolas, Sliwa, Michel, Woodhouse, Joyce, Schirò, Giorgio, Adam, Virgile, Aquila, Andrew, Barends, Thomas R. M., Boutet, Sébastien, Byrdin, Martin, Carbajo, Sergio, De la Mora, Eugenio, Doak, R. Bruce, Feliks, Mikolaj, Fieschi, Franck, Foucar, Lutz, Guillon, Virginia, Hilpert, Mario, Hunter, Mark S., Jakobs, Stefan, Koglin, Jason E., Kovacsova, Gabriela, Lane, Thomas J., Lévy, Bernard, Liang, Mengning, Nass, Karol, Ridard, Jacqueline, Robinson, Joseph S., Roome, Christopher M., Ruckebusch, Cyril, Seaberg, Matthew, Thepaut, Michel, Cammarata, Marco, Demachy, Isabelle, Field, Martin, Shoeman, Robert L., Bourgeois, Dominique, Colletier, Jacques-Philippe, Schlichting, Ilme, & Weik, Martin. Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography. United States. https://doi.org/10.1038/nchem.2853
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Coquelle, Nicolas, Sliwa, Michel, Woodhouse, Joyce, Schirò, Giorgio, Adam, Virgile, Aquila, Andrew, Barends, Thomas R. M., Boutet, Sébastien, Byrdin, Martin, Carbajo, Sergio, De la Mora, Eugenio, Doak, R. Bruce, Feliks, Mikolaj, Fieschi, Franck, Foucar, Lutz, Guillon, Virginia, Hilpert, Mario, Hunter, Mark S., Jakobs, Stefan, Koglin, Jason E., Kovacsova, Gabriela, Lane, Thomas J., Lévy, Bernard, Liang, Mengning, Nass, Karol, Ridard, Jacqueline, Robinson, Joseph S., Roome, Christopher M., Ruckebusch, Cyril, Seaberg, Matthew, Thepaut, Michel, Cammarata, Marco, Demachy, Isabelle, Field, Martin, Shoeman, Robert L., Bourgeois, Dominique, Colletier, Jacques-Philippe, Schlichting, Ilme, and Weik, Martin. Mon . "Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography". United States. https://doi.org/10.1038/nchem.2853. https://www.osti.gov/servlets/purl/1426209.
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@article{osti_1426209,
title = {Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography},
author = {Coquelle, Nicolas and Sliwa, Michel and Woodhouse, Joyce and Schirò, Giorgio and Adam, Virgile and Aquila, Andrew and Barends, Thomas R. M. and Boutet, Sébastien and Byrdin, Martin and Carbajo, Sergio and De la Mora, Eugenio and Doak, R. Bruce and Feliks, Mikolaj and Fieschi, Franck and Foucar, Lutz and Guillon, Virginia and Hilpert, Mario and Hunter, Mark S. and Jakobs, Stefan and Koglin, Jason E. and Kovacsova, Gabriela and Lane, Thomas J. and Lévy, Bernard and Liang, Mengning and Nass, Karol and Ridard, Jacqueline and Robinson, Joseph S. and Roome, Christopher M. and Ruckebusch, Cyril and Seaberg, Matthew and Thepaut, Michel and Cammarata, Marco and Demachy, Isabelle and Field, Martin and Shoeman, Robert L. and Bourgeois, Dominique and Colletier, Jacques-Philippe and Schlichting, Ilme and Weik, Martin},
abstractNote = {Chromophores absorb light in photosensitive proteins and thereby initiate fundamental biological processes such as photosynthesis, vision and biofluorescence. An important goal in their understanding is the provision of detailed structural descriptions of the ultrafast photochemical events that they undergo, in particular of the excited states that connect chemistry to biological function. Here in this paper we report on the structures of two excited states in the reversibly photoswitchable fluorescent protein rsEGFP2. We populated the states through femtosecond illumination of rsEGFP2 in its non-fluorescent off state and observed their build-up (within less than one picosecond) and decay (on the several picosecond timescale). Using an X-ray free-electron laser, we performed picosecond time-resolved crystallography and show that the hydroxybenzylidene imidazolinone chromophore in one of the excited states assumes a near-canonical twisted configuration halfway between the trans and cis isomers. This is in line with excited-state quantum mechanics/molecular mechanics and classical molecular dynamics simulations. Our new understanding of the structure around the twisted chromophore enabled the design of a mutant that displays a twofold increase in its off-to-on photoswitching quantum yield.},
doi = {10.1038/nchem.2853},
journal = {Nature Chemistry},
number = 1,
volume = 10,
place = {United States},
year = {2017},
month = {9}
}
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