Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin

Nass Kovacs, Gabriela; Colletier, Jacques-Philippe; Grünbein, Marie Luise; Yang, Yang; Stensitzki, Till; Batyuk, Alexander; Carbajo, Sergio; Doak, R. Bruce; Ehrenberg, David; Foucar, Lutz; Gasper, Raphael; Gorel, Alexander; Hilpert, Mario; Kloos, Marco; Koglin, Jason E.; Reinstein, Jochen; Roome, Christopher M.; Schlesinger, Ramona; Seaberg, Matthew; Shoeman, Robert L.; Stricker, Miriam; Boutet, Sébastien; Haacke, Stefan; Heberle, Joachim; Heyne, Karsten; Domratcheva, Tatiana; Barends, Thomas R.  M.; Schlichting, Ilme

doi:10.1038/s41467-019-10758-0

Title: Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin

Abstract

Bacteriorhodopsin (bR) is a light-driven proton pump. The primary photochemical event upon light absorption is isomerization of the retinal chromophore. Here we used time-resolved crystallography at an X-ray free-electron laser to follow the structural changes in multiphoton-excited bR from 250 femtoseconds to 10 picoseconds. Quantum chemistry and ultrafast spectroscopy were used to identify a sequential two-photon absorption process, leading to excitation of a tryptophan residue flanking the retinal chromophore, as a first manifestation of multiphoton effects. We resolve distinct stages in the structural dynamics of the all-trans retinal in photoexcited bR to a highly twisted 13-cis conformation. Other active site sub-picosecond rearrangements include correlated vibrational motions of the electronically excited retinal chromophore, the surrounding amino acids and water molecules as well as their hydrogen bonding network. These results show that this extended photo-active network forms an electronically and vibrationally coupled system in bR, and most likely in all retinal proteins.

Authors:

Nass Kovacs, Gabriela ^[1]; Colletier, Jacques-Philippe ^[2]; Grünbein, Marie Luise ^[1]; Yang, Yang ^[3];

^[3];

^[4]; Carbajo, Sergio ^[4]; Doak, R. Bruce ^[1]; Ehrenberg, David ^[3]; Foucar, Lutz ^[1]; Gasper, Raphael ^[5]; Gorel, Alexander ^[1]; Hilpert, Mario ^[1]; Kloos, Marco ^[1];

^[4]; Reinstein, Jochen ^[1]; Roome, Christopher M. ^[1];

^[3];

^[4];

^[1] more »

Max-Planck-Inst. für Medizinische Forschung, Heidelberg (Germany)
Univ. Grenoble Alpes, Grenoble (France)
Freie Univ. Berlin, Berlin (Germany)
SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
Max-Planck-Inst. für Molekulare Physiologie, Dortmund (Germany)
Univ. de Strasbourg-CNRS, Strasbourg (France)

Publication Date:: Thu Jul 18 00:00:00 EDT 2019

Research Org.:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Org.:: USDOE

OSTI Identifier:: 1546794

Grant/Contract Number:: AC02-76SF00515; ANR-17-CE11-0018-01

Resource Type:: Accepted Manuscript

Journal Name:: Nature Communications

Additional Journal Information:: Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2041-1723

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

Subject:: 71 CLASSICAL AND QUANTUM MECHANICS, GENERAL PHYSICS

Citation Formats


                    Nass Kovacs, Gabriela, Colletier, Jacques-Philippe, Grünbein, Marie Luise, Yang, Yang, Stensitzki, Till, Batyuk, Alexander, Carbajo, Sergio, Doak, R. Bruce, Ehrenberg, David, Foucar, Lutz, Gasper, Raphael, Gorel, Alexander, Hilpert, Mario, Kloos, Marco, Koglin, Jason E., Reinstein, Jochen, Roome, Christopher M., Schlesinger, Ramona, Seaberg, Matthew, Shoeman, Robert L., Stricker, Miriam, Boutet, Sébastien, Haacke, Stefan, Heberle, Joachim, Heyne, Karsten, Domratcheva, Tatiana, Barends, Thomas R.  M., and Schlichting, Ilme. Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin.  United States: N. p., 2019. 
Web.  doi:10.1038/s41467-019-10758-0.

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                    Nass Kovacs, Gabriela, Colletier, Jacques-Philippe, Grünbein, Marie Luise, Yang, Yang, Stensitzki, Till, Batyuk, Alexander, Carbajo, Sergio, Doak, R. Bruce, Ehrenberg, David, Foucar, Lutz, Gasper, Raphael, Gorel, Alexander, Hilpert, Mario, Kloos, Marco, Koglin, Jason E., Reinstein, Jochen, Roome, Christopher M., Schlesinger, Ramona, Seaberg, Matthew, Shoeman, Robert L., Stricker, Miriam, Boutet, Sébastien, Haacke, Stefan, Heberle, Joachim, Heyne, Karsten, Domratcheva, Tatiana, Barends, Thomas R.  M., & Schlichting, Ilme. Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin.  United States.  https://doi.org/10.1038/s41467-019-10758-0

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                    Nass Kovacs, Gabriela, Colletier, Jacques-Philippe, Grünbein, Marie Luise, Yang, Yang, Stensitzki, Till, Batyuk, Alexander, Carbajo, Sergio, Doak, R. Bruce, Ehrenberg, David, Foucar, Lutz, Gasper, Raphael, Gorel, Alexander, Hilpert, Mario, Kloos, Marco, Koglin, Jason E., Reinstein, Jochen, Roome, Christopher M., Schlesinger, Ramona, Seaberg, Matthew, Shoeman, Robert L., Stricker, Miriam, Boutet, Sébastien, Haacke, Stefan, Heberle, Joachim, Heyne, Karsten, Domratcheva, Tatiana, Barends, Thomas R.  M., and Schlichting, Ilme. Thu .  
"Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin".  United States.  https://doi.org/10.1038/s41467-019-10758-0.  https://www.osti.gov/servlets/purl/1546794.

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@article{osti_1546794,

  title        = {Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin},

  author       = {Nass Kovacs, Gabriela and Colletier, Jacques-Philippe and Grünbein, Marie Luise and Yang, Yang and Stensitzki, Till and Batyuk, Alexander and Carbajo, Sergio and Doak, R. Bruce and Ehrenberg, David and Foucar, Lutz and Gasper, Raphael and Gorel, Alexander and Hilpert, Mario and Kloos, Marco and Koglin, Jason E. and Reinstein, Jochen and Roome, Christopher M. and Schlesinger, Ramona and Seaberg, Matthew and Shoeman, Robert L. and Stricker, Miriam and Boutet, Sébastien and Haacke, Stefan and Heberle, Joachim and Heyne, Karsten and Domratcheva, Tatiana and Barends, Thomas R.  M. and Schlichting, Ilme},

  abstractNote = {Bacteriorhodopsin (bR) is a light-driven proton pump. The primary photochemical event upon light absorption is isomerization of the retinal chromophore. Here we used time-resolved crystallography at an X-ray free-electron laser to follow the structural changes in multiphoton-excited bR from 250 femtoseconds to 10 picoseconds. Quantum chemistry and ultrafast spectroscopy were used to identify a sequential two-photon absorption process, leading to excitation of a tryptophan residue flanking the retinal chromophore, as a first manifestation of multiphoton effects. We resolve distinct stages in the structural dynamics of the all-trans retinal in photoexcited bR to a highly twisted 13-cis conformation. Other active site sub-picosecond rearrangements include correlated vibrational motions of the electronically excited retinal chromophore, the surrounding amino acids and water molecules as well as their hydrogen bonding network. These results show that this extended photo-active network forms an electronically and vibrationally coupled system in bR, and most likely in all retinal proteins.},

  doi          = {10.1038/s41467-019-10758-0},

  journal      = {Nature Communications},

  number       = 1,

  volume       = 10,

  place        = {United States},

  year         = {Thu Jul 18 00:00:00 EDT 2019},

  month        = {Thu Jul 18 00:00:00 EDT 2019}

}

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Works referencing / citing this record:

A tool for visualizing protein motions in time-resolved crystallography
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