Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin

Gabriela Nass Kovacs, Jacques-Philippe Colletier, Marie Luise Grünbein, Yang Yang, Till Stensitzki, Alexander Batyuk, Sergio Carbajo, R. Bruce Doak, David Ehrenberg, Lutz Foucar, Raphael Gasper, Alexander Gorel, Mario Hilpert, Marco Kloos, Jason E. Koglin, Jochen Reinstein, Christopher M. Roome, Ramona Schlesinger, Matthew Seaberg, Robert L. Shoeman, Miriam Stricker, Sébastien Boutet, Stefan Haacke, Joachim Heberle, Karsten Heyne, Tatiana Domratcheva (), Thomas R. M. Barends and Ilme Schlichting ()
Additional contact information
Gabriela Nass Kovacs: Max-Planck-Institut für Medizinische Forschung
Jacques-Philippe Colletier: Univ. Grenoble Alpes, CNRS, CEA, Institut de Biologie Structurale
Marie Luise Grünbein: Max-Planck-Institut für Medizinische Forschung
Yang Yang: Freie Universität Berlin, Department of Physics
Till Stensitzki: Freie Universität Berlin, Department of Physics
Alexander Batyuk: Linac Coherent Light Source (LCLS), SLAC National Accelerator Laboratory
Sergio Carbajo: Linac Coherent Light Source (LCLS), SLAC National Accelerator Laboratory
R. Bruce Doak: Max-Planck-Institut für Medizinische Forschung
David Ehrenberg: Freie Universität Berlin, Department of Physics
Lutz Foucar: Max-Planck-Institut für Medizinische Forschung
Raphael Gasper: Max-Planck-Institut für Molekulare Physiologie
Alexander Gorel: Max-Planck-Institut für Medizinische Forschung
Mario Hilpert: Max-Planck-Institut für Medizinische Forschung
Marco Kloos: Max-Planck-Institut für Medizinische Forschung
Jason E. Koglin: Linac Coherent Light Source (LCLS), SLAC National Accelerator Laboratory
Jochen Reinstein: Max-Planck-Institut für Medizinische Forschung
Christopher M. Roome: Max-Planck-Institut für Medizinische Forschung
Ramona Schlesinger: Freie Universität Berlin, Department of Physics
Matthew Seaberg: Linac Coherent Light Source (LCLS), SLAC National Accelerator Laboratory
Robert L. Shoeman: Max-Planck-Institut für Medizinische Forschung
Miriam Stricker: Max-Planck-Institut für Medizinische Forschung
Sébastien Boutet: Linac Coherent Light Source (LCLS), SLAC National Accelerator Laboratory
Stefan Haacke: Université de Strasbourg-CNRS, UMR 7504, IPCMS
Joachim Heberle: Freie Universität Berlin, Department of Physics
Karsten Heyne: Freie Universität Berlin, Department of Physics
Tatiana Domratcheva: Max-Planck-Institut für Medizinische Forschung
Thomas R. M. Barends: Max-Planck-Institut für Medizinische Forschung
Ilme Schlichting: Max-Planck-Institut für Medizinische Forschung

Nature Communications, 2019, vol. 10, issue 1, 1-17

Abstract: 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.

Date: 2019
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DOI: 10.1038/s41467-019-10758-0

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