skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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:
 [1];  [2];  [1];  [3]; ORCiD logo [3]; ORCiD logo [4];  [4];  [1];  [3];  [1];  [5];  [1];  [1];  [1]; ORCiD logo [4];  [1];  [1]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [1] more »; ORCiD logo [1];  [4]; ORCiD logo [6];  [3];  [3];  [1];  [1]; ORCiD logo [1] « less
  1. Max-Planck-Inst. für Medizinische Forschung, Heidelberg (Germany)
  2. Univ. Grenoble Alpes, Grenoble (France)
  3. Freie Univ. Berlin, Berlin (Germany)
  4. SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
  5. Max-Planck-Inst. für Molekulare Physiologie, Dortmund (Germany)
  6. Univ. de Strasbourg-CNRS, Strasbourg (France)
Publication Date:
Research Org.:
SLAC National Accelerator Lab., 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.
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. doi:10.1038/s41467-019-10758-0.
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. doi:10.1038/s41467-019-10758-0. https://www.osti.gov/servlets/purl/1546794.
@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 = {2019},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 6 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Vibrationally coherent photochemistry in the femtosecond primary event of vision
journal, October 1994


Functions of a New Photoreceptor Membrane
journal, October 1973

  • Oesterhelt, D.; Stoeckenius, W.
  • Proceedings of the National Academy of Sciences, Vol. 70, Issue 10
  • DOI: 10.1073/pnas.70.10.2853

Proton transfers in the bacteriorhodopsin photocycle
journal, August 2006


Real-time spectroscopy of transition states in bacteriorhodopsin during retinal isomerization
journal, November 2001

  • Kobayashi, Takayoshi; Saito, Takashi; Ohtani, Hiroyuki
  • Nature, Vol. 414, Issue 6863
  • DOI: 10.1038/35107042

Femtosecond Infrared Spectroscopy of Bacteriorhodopsin Chromophore Isomerization
journal, August 2002


Theory and Simulation of the Ultrafast Double-Bond Isomerization of Biological Chromophores
journal, October 2017


Excited-state reaction dynamics of bacteriorhodopsin studied by femtosecond spectroscopy
journal, February 1988


Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser
journal, June 2018


The primary photoreaction of channelrhodopsin-1: wavelength dependent photoreactions induced by ground-state heterogeneity
journal, July 2015

  • Stensitzki, Till; Muders, Vera; Schlesinger, Ramona
  • Frontiers in Molecular Biosciences, Vol. 2
  • DOI: 10.3389/fmolb.2015.00041

Excited-state dynamics of bacteriorhodopsin probed by broadband femtosecond fluorescence spectroscopy
journal, January 2005

  • Schmidt, B.; Sobotta, C.; Heinz, B.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1706, Issue 1-2
  • DOI: 10.1016/j.bbabio.2004.10.008

Control of retinal isomerization in bacteriorhodopsin in the high-intensity regime
journal, June 2009

  • Florean, A. C.; Cardoza, D.; White, J. L.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 27
  • DOI: 10.1073/pnas.0904589106

Resonant Two-Photon Excitation Pathways During Retinal-Isomerization in Bacteriorhodopsin
journal, January 2013


Energy transfer from retinal to amino acids — a time-resolved study of the ultraviolet emission of bacteriorhodopsin
journal, October 1986

  • Polland, H. J.; Franz, M. A.; Zinth, W.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 851, Issue 3
  • DOI: 10.1016/0005-2728(86)90077-0

Formation dynamics and nature of tryptophan's primary photoproduct in aqueous solution
journal, January 2010

  • Léonard, J.; Sharma, D.; Szafarowicz, B.
  • Physical Chemistry Chemical Physics, Vol. 12, Issue 48
  • DOI: 10.1039/c0cp00615g

Measurements of the driving forces of bio-motors using the fluctuation theorem
journal, January 2012


First-Order Interacting Space Approach to Excited-State Molecular Interaction: Solvatochromic Shift of p -Coumaric Acid and Retinal Schiff Base
journal, May 2018

  • Yanai, Kazuma; Ishimura, Kazuya; Nakayama, Akira
  • Journal of Chemical Theory and Computation, Vol. 14, Issue 7
  • DOI: 10.1021/acs.jctc.7b01089

Aborted double bicycle-pedal isomerization with hydrogen bond breaking is the primary event of bacteriorhodopsin proton pumping
journal, November 2010

  • Altoe, P.; Cembran, A.; Olivucci, M.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 47
  • DOI: 10.1073/pnas.1007000107

Functional electric field changes in photoactivated proteins revealed by ultrafast Stark spectroscopy of the Trp residues
journal, April 2009

  • Leonard, J.; Portuondo-Campa, E.; Cannizzo, A.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 19
  • DOI: 10.1073/pnas.0812877106

Sub-nanosecond tryptophan radical deprotonation mediated by a protein-bound water cluster in class II DNA photolyases
journal, January 2018

  • Müller, Pavel; Ignatz, Elisabeth; Kiontke, Stephan
  • Chemical Science, Vol. 9, Issue 5
  • DOI: 10.1039/C7SC03969G

Microsecond Light-Induced Proton Transfer to Flavin in the Blue Light Sensor Plant Cryptochrome
journal, October 2009

  • Langenbacher, Thomas; Immeln, Dominik; Dick, Bernhard
  • Journal of the American Chemical Society, Vol. 131, Issue 40
  • DOI: 10.1021/ja901628y

Oxidation of tryptophan and N-methylindole by N3.cntdot., Br2.-, and (SCN)2.- radicals in light- and heavy-water solutions: a pulse radiolysis study
journal, May 1991

  • Solar, Sonja; Getoff, Nikola; Surdhar, Parminder S.
  • The Journal of Physical Chemistry, Vol. 95, Issue 9
  • DOI: 10.1021/j100162a038

A three-dimensional movie of structural changes in bacteriorhodopsin
journal, December 2016

  • Nango, Eriko; Royant, Antoine; Kubo, Minoru
  • Science, Vol. 354, Issue 6319, p. 1552-1557
  • DOI: 10.1126/science.aah3497

Room-temperature serial crystallography at synchrotron X-ray sources using slowly flowing free-standing high-viscosity microstreams
journal, January 2015

  • Botha, Sabine; Nass, Karol; Barends, Thomas R. M.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 2
  • DOI: 10.1107/S1399004714026327

The Coherent X-ray Imaging instrument at the Linac Coherent Light Source
journal, April 2015

  • Liang, Mengning; Williams, Garth J.; Messerschmidt, Marc
  • Journal of Synchrotron Radiation, Vol. 22, Issue 3
  • DOI: 10.1107/S160057751500449X

Application of Singular Value Decomposition to the Analysis of Time-Resolved Macromolecular X-Ray Data
journal, March 2003


Femtosecond structural dynamics drives the trans/cis isomerization in photoactive yellow protein
journal, May 2016


Femtosecond Time-Resolved Stimulated Raman Reveals the Birth of Bacteriorhodopsin’s J and K Intermediates
journal, June 2009

  • Shim, Sangdeok; Dasgupta, Jyotishman; Mathies, Richard A.
  • Journal of the American Chemical Society, Vol. 131, Issue 22
  • DOI: 10.1021/ja809137x

Removal of methyl groups from retinal controls the activity of bacteriorhodopsin
journal, May 1983

  • Gaertner, Wolfgang; Towner, Paul; Hopf, Henning
  • Biochemistry, Vol. 22, Issue 11
  • DOI: 10.1021/bi00280a007

Primary Step in Bacteriorhodopsin Photosynthesis:  Bond Stretch Rather than Angle Twist of Its Retinal Excited-State Structure
journal, September 1998

  • Song, Li; El-Sayed, M. A.
  • Journal of the American Chemical Society, Vol. 120, Issue 34
  • DOI: 10.1021/ja980390d

Following Photoinduced Dynamics in Bacteriorhodopsin with 7-fs Impulsive Vibrational Spectroscopy
journal, January 2007

  • Kahan, Anat; Nahmias, Omer; Friedman, Noga
  • Journal of the American Chemical Society, Vol. 129, Issue 3
  • DOI: 10.1021/ja064910d

Comparing photoinduced vibrational coherences in bacteriorhodopsin and in native and locked retinal protonated Schiff bases
journal, November 2003


Probing Ultrafast Photochemistry of Retinal Proteins in the Near-IR: Bacteriorhodopsin and Anabaena Sensory Rhodopsin vs Retinal Protonated Schiff Base in Solution
journal, November 2012

  • Wand, Amir; Loevsky, Boris; Friedman, Noga
  • The Journal of Physical Chemistry B, Vol. 117, Issue 16
  • DOI: 10.1021/jp309189y

Asymmetric Toggling of a Natural Photoswitch: Ultrafast Spectroscopy of Anabaena Sensory Rhodopsin
journal, December 2011

  • Wand, Amir; Rozin, Rinat; Eliash, Tamar
  • Journal of the American Chemical Society, Vol. 133, Issue 51
  • DOI: 10.1021/ja208371g

Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation
journal, September 2015


Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography
journal, September 2017

  • Coquelle, Nicolas; Sliwa, Michel; Woodhouse, Joyce
  • Nature Chemistry, Vol. 10, Issue 1
  • DOI: 10.1038/nchem.2853

Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser
journal, August 2014

  • Arnlund, David; Johansson, Linda C.; Wickstrand, Cecilia
  • Nature Methods, Vol. 11, Issue 9
  • DOI: 10.1038/nmeth.3067

Viscous hydrophilic injection matrices for serial crystallography
journal, May 2017


Lipidic cubic phase serial millisecond crystallography using synchrotron radiation
journal, March 2015


Preparation of microcrystals in lipidic cubic phase for serial femtosecond crystallography
journal, August 2014


Light-dark adaptation of bacteriorhodopsin in Triton-treated purple membrane
journal, March 1980

  • Casadio, R.; Gutowitz, H.; Mowery, P.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 590, Issue 1
  • DOI: 10.1016/0005-2728(80)90142-5

Retinal isomer ratio in dark-adapted purple membrane and bacteriorhodopsin monomers
journal, January 1989

  • Scherrer, P.; Mathew, M. K.; Sperling, W.
  • Biochemistry, Vol. 28, Issue 2
  • DOI: 10.1021/bi00428a063

X-ray detectors at the Linac Coherent Light Source
journal, April 2015

  • Blaj, Gabriel; Caragiulo, Pietro; Carini, Gabriella
  • Journal of Synchrotron Radiation, Vol. 22, Issue 3
  • DOI: 10.1107/S1600577515005317

CASS—CFEL-ASG software suite
journal, October 2012

  • Foucar, Lutz; Barty, Anton; Coppola, Nicola
  • Computer Physics Communications, Vol. 183, Issue 10
  • DOI: 10.1016/j.cpc.2012.04.023

Spectral encoding of x-ray/optical relative delay
journal, January 2011

  • Bionta, Mina R.; Lemke, H. T.; Cryan, J. P.
  • Optics Express, Vol. 19, Issue 22
  • DOI: 10.1364/OE.19.021855

CrystFEL : a software suite for snapshot serial crystallography
journal, March 2012

  • White, Thomas A.; Kirian, Richard A.; Martin, Andrew V.
  • Journal of Applied Crystallography, Vol. 45, Issue 2
  • DOI: 10.1107/S0021889812002312

Improved Estimation of Structure-Factor Difference Amplitudesfrom Poorly Accurate Data
journal, September 1997

  • Ursby, T.; Bourgeois, D.
  • Acta Crystallographica Section A Foundations of Crystallography, Vol. 53, Issue 5
  • DOI: 10.1107/S0108767397004522

Structure-factor extrapolation using the scalar approximation: theory, applications and limitations
journal, September 2007

  • Genick, Ulrich K.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 10
  • DOI: 10.1107/S0907444907038164

PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010

  • Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
  • DOI: 10.1107/S0907444909052925

Coot model-building tools for molecular graphics
journal, November 2004

  • Emsley, Paul; Cowtan, Kevin
  • Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
  • DOI: 10.1107/S0907444904019158

Generation, shaping, and characterization of intense femtosecond pulses tunable from 3 to 20 μm
journal, January 2000

  • Kaindl, Robert A.; Wurm, Matthias; Reimann, Klaus
  • Journal of the Optical Society of America B, Vol. 17, Issue 12, p. 2086-2094
  • DOI: 10.1364/JOSAB.17.002086

Gaussian basis sets for use in correlated molecular calculations. V. Core‐valence basis sets for boron through neon
journal, September 1995

  • Woon, David E.; Dunning, Thom H.
  • The Journal of Chemical Physics, Vol. 103, Issue 11
  • DOI: 10.1063/1.470645

Density‐functional thermochemistry. III. The role of exact exchange
journal, April 1993

  • Becke, Axel D.
  • The Journal of Chemical Physics, Vol. 98, Issue 7, p. 5648-5652
  • DOI: 10.1063/1.464913

Extended multi-configuration quasi-degenerate perturbation theory: The new approach to multi-state multi-reference perturbation theory
journal, June 2011

  • Granovsky, Alexander A.
  • The Journal of Chemical Physics, Vol. 134, Issue 21
  • DOI: 10.1063/1.3596699

Intruder state avoidance multireference Møller-Plesset perturbation theory: Multireference Møller-Plesset Perturbation Theory
journal, May 2002

  • Witek, Henryk A.; Choe, Yoong-Kee; Finley, James P.
  • Journal of Computational Chemistry, Vol. 23, Issue 10
  • DOI: 10.1002/jcc.10098

Generalization of the Mulliken-Hush treatment for the calculation of electron transfer matrix elements
journal, January 1996


General atomic and molecular electronic structure system
journal, November 1993

  • Schmidt, Michael W.; Baldridge, Kim K.; Boatz, Jerry A.
  • Journal of Computational Chemistry, Vol. 14, Issue 11, p. 1347-1363
  • DOI: 10.1002/jcc.540141112

    Works referencing / citing this record:

    Intruder state avoidance multireference Møller-Plesset perturbation theory: Multireference Møller-Plesset Perturbation Theory
    journal, May 2002

    • Witek, Henryk A.; Choe, Yoong-Kee; Finley, James P.
    • Journal of Computational Chemistry, Vol. 23, Issue 10
    • DOI: 10.1002/jcc.10098

    General atomic and molecular electronic structure system
    journal, November 1993

    • Schmidt, Michael W.; Baldridge, Kim K.; Boatz, Jerry A.
    • Journal of Computational Chemistry, Vol. 14, Issue 11, p. 1347-1363
    • DOI: 10.1002/jcc.540141112

    Light-dark adaptation of bacteriorhodopsin in Triton-treated purple membrane
    journal, March 1980

    • Casadio, R.; Gutowitz, H.; Mowery, P.
    • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 590, Issue 1
    • DOI: 10.1016/0005-2728(80)90142-5

    Energy transfer from retinal to amino acids — a time-resolved study of the ultraviolet emission of bacteriorhodopsin
    journal, October 1986

    • Polland, H. J.; Franz, M. A.; Zinth, W.
    • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 851, Issue 3
    • DOI: 10.1016/0005-2728(86)90077-0

    Excited-state reaction dynamics of bacteriorhodopsin studied by femtosecond spectroscopy
    journal, February 1988


    Generalization of the Mulliken-Hush treatment for the calculation of electron transfer matrix elements
    journal, January 1996


    Excited-state dynamics of bacteriorhodopsin probed by broadband femtosecond fluorescence spectroscopy
    journal, January 2005

    • Schmidt, B.; Sobotta, C.; Heinz, B.
    • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1706, Issue 1-2
    • DOI: 10.1016/j.bbabio.2004.10.008

    Proton transfers in the bacteriorhodopsin photocycle
    journal, August 2006


    CASS—CFEL-ASG software suite
    journal, October 2012

    • Foucar, Lutz; Barty, Anton; Coppola, Nicola
    • Computer Physics Communications, Vol. 183, Issue 10
    • DOI: 10.1016/j.cpc.2012.04.023

    Comparing photoinduced vibrational coherences in bacteriorhodopsin and in native and locked retinal protonated Schiff bases
    journal, November 2003


    Theory and Simulation of the Ultrafast Double-Bond Isomerization of Biological Chromophores
    journal, October 2017


    First-Order Interacting Space Approach to Excited-State Molecular Interaction: Solvatochromic Shift of p -Coumaric Acid and Retinal Schiff Base
    journal, May 2018

    • Yanai, Kazuma; Ishimura, Kazuya; Nakayama, Akira
    • Journal of Chemical Theory and Computation, Vol. 14, Issue 7
    • DOI: 10.1021/acs.jctc.7b01089

    Removal of methyl groups from retinal controls the activity of bacteriorhodopsin
    journal, May 1983

    • Gaertner, Wolfgang; Towner, Paul; Hopf, Henning
    • Biochemistry, Vol. 22, Issue 11
    • DOI: 10.1021/bi00280a007

    Retinal isomer ratio in dark-adapted purple membrane and bacteriorhodopsin monomers
    journal, January 1989

    • Scherrer, P.; Mathew, M. K.; Sperling, W.
    • Biochemistry, Vol. 28, Issue 2
    • DOI: 10.1021/bi00428a063

    Oxidation of tryptophan and N-methylindole by N3.cntdot., Br2.-, and (SCN)2.- radicals in light- and heavy-water solutions: a pulse radiolysis study
    journal, May 1991

    • Solar, Sonja; Getoff, Nikola; Surdhar, Parminder S.
    • The Journal of Physical Chemistry, Vol. 95, Issue 9
    • DOI: 10.1021/j100162a038

    Following Photoinduced Dynamics in Bacteriorhodopsin with 7-fs Impulsive Vibrational Spectroscopy
    journal, January 2007

    • Kahan, Anat; Nahmias, Omer; Friedman, Noga
    • Journal of the American Chemical Society, Vol. 129, Issue 3
    • DOI: 10.1021/ja064910d

    Asymmetric Toggling of a Natural Photoswitch: Ultrafast Spectroscopy of Anabaena Sensory Rhodopsin
    journal, December 2011

    • Wand, Amir; Rozin, Rinat; Eliash, Tamar
    • Journal of the American Chemical Society, Vol. 133, Issue 51
    • DOI: 10.1021/ja208371g

    Femtosecond Time-Resolved Stimulated Raman Reveals the Birth of Bacteriorhodopsin’s J and K Intermediates
    journal, June 2009

    • Shim, Sangdeok; Dasgupta, Jyotishman; Mathies, Richard A.
    • Journal of the American Chemical Society, Vol. 131, Issue 22
    • DOI: 10.1021/ja809137x

    Microsecond Light-Induced Proton Transfer to Flavin in the Blue Light Sensor Plant Cryptochrome
    journal, October 2009

    • Langenbacher, Thomas; Immeln, Dominik; Dick, Bernhard
    • Journal of the American Chemical Society, Vol. 131, Issue 40
    • DOI: 10.1021/ja901628y

    Primary Step in Bacteriorhodopsin Photosynthesis:  Bond Stretch Rather than Angle Twist of Its Retinal Excited-State Structure
    journal, September 1998

    • Song, Li; El-Sayed, M. A.
    • Journal of the American Chemical Society, Vol. 120, Issue 34
    • DOI: 10.1021/ja980390d

    Probing Ultrafast Photochemistry of Retinal Proteins in the Near-IR: Bacteriorhodopsin and Anabaena Sensory Rhodopsin vs Retinal Protonated Schiff Base in Solution
    journal, November 2012

    • Wand, Amir; Loevsky, Boris; Friedman, Noga
    • The Journal of Physical Chemistry B, Vol. 117, Issue 16
    • DOI: 10.1021/jp309189y

    Real-time spectroscopy of transition states in bacteriorhodopsin during retinal isomerization
    journal, November 2001

    • Kobayashi, Takayoshi; Saito, Takashi; Ohtani, Hiroyuki
    • Nature, Vol. 414, Issue 6863
    • DOI: 10.1038/35107042

    Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography
    journal, September 2017

    • Coquelle, Nicolas; Sliwa, Michel; Woodhouse, Joyce
    • Nature Chemistry, Vol. 10, Issue 1
    • DOI: 10.1038/nchem.2853

    Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser
    journal, August 2014

    • Arnlund, David; Johansson, Linda C.; Wickstrand, Cecilia
    • Nature Methods, Vol. 11, Issue 9
    • DOI: 10.1038/nmeth.3067

    Preparation of microcrystals in lipidic cubic phase for serial femtosecond crystallography
    journal, August 2014


    Formation dynamics and nature of tryptophan's primary photoproduct in aqueous solution
    journal, January 2010

    • Léonard, J.; Sharma, D.; Szafarowicz, B.
    • Physical Chemistry Chemical Physics, Vol. 12, Issue 48
    • DOI: 10.1039/c0cp00615g

    Resonant Two-Photon Excitation Pathways During Retinal-Isomerization in Bacteriorhodopsin
    journal, January 2013


    Extended multi-configuration quasi-degenerate perturbation theory: The new approach to multi-state multi-reference perturbation theory
    journal, June 2011

    • Granovsky, Alexander A.
    • The Journal of Chemical Physics, Vol. 134, Issue 21
    • DOI: 10.1063/1.3596699

    Density‐functional thermochemistry. III. The role of exact exchange
    journal, April 1993

    • Becke, Axel D.
    • The Journal of Chemical Physics, Vol. 98, Issue 7, p. 5648-5652
    • DOI: 10.1063/1.464913

    Gaussian basis sets for use in correlated molecular calculations. V. Core‐valence basis sets for boron through neon
    journal, September 1995

    • Woon, David E.; Dunning, Thom H.
    • The Journal of Chemical Physics, Vol. 103, Issue 11
    • DOI: 10.1063/1.470645

    Functional electric field changes in photoactivated proteins revealed by ultrafast Stark spectroscopy of the Trp residues
    journal, April 2009

    • Leonard, J.; Portuondo-Campa, E.; Cannizzo, A.
    • Proceedings of the National Academy of Sciences, Vol. 106, Issue 19
    • DOI: 10.1073/pnas.0812877106

    Control of retinal isomerization in bacteriorhodopsin in the high-intensity regime
    journal, June 2009

    • Florean, A. C.; Cardoza, D.; White, J. L.
    • Proceedings of the National Academy of Sciences, Vol. 106, Issue 27
    • DOI: 10.1073/pnas.0904589106

    Aborted double bicycle-pedal isomerization with hydrogen bond breaking is the primary event of bacteriorhodopsin proton pumping
    journal, November 2010

    • Altoe, P.; Cembran, A.; Olivucci, M.
    • Proceedings of the National Academy of Sciences, Vol. 107, Issue 47
    • DOI: 10.1073/pnas.1007000107

    Functions of a New Photoreceptor Membrane
    journal, October 1973

    • Oesterhelt, D.; Stoeckenius, W.
    • Proceedings of the National Academy of Sciences, Vol. 70, Issue 10
    • DOI: 10.1073/pnas.70.10.2853

    Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density
    journal, January 1988


    Femtosecond Infrared Spectroscopy of Bacteriorhodopsin Chromophore Isomerization
    journal, August 2002


    Vibrationally coherent photochemistry in the femtosecond primary event of vision
    journal, October 1994


    Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation
    journal, September 2015


    Femtosecond structural dynamics drives the trans/cis isomerization in photoactive yellow protein
    journal, May 2016


    A three-dimensional movie of structural changes in bacteriorhodopsin
    journal, December 2016

    • Nango, Eriko; Royant, Antoine; Kubo, Minoru
    • Science, Vol. 354, Issue 6319, p. 1552-1557
    • DOI: 10.1126/science.aah3497

    Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser
    journal, June 2018


    Measurements of the driving forces of bio-motors using the fluctuation theorem
    journal, January 2012


    The primary photoreaction of channelrhodopsin-1: wavelength dependent photoreactions induced by ground-state heterogeneity
    journal, July 2015

    • Stensitzki, Till; Muders, Vera; Schlesinger, Ramona
    • Frontiers in Molecular Biosciences, Vol. 2
    • DOI: 10.3389/fmolb.2015.00041