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Title: Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser

Abstract

Ultrafast isomerization of retinal is the primary step in photoresponsive biological functions including vision in humans and ion transport across bacterial membranes. In this study, we used an x-ray laser to study the subpicosecond structural dynamics of retinal isomerization in the light-driven proton pump bacteriorhodopsin. A series of structural snapshots with near-atomic spatial resolution and temporal resolution in the femtosecond regime show how the excited all-trans retinal samples conformational states within the protein binding pocket before passing through a twisted geometry and emerging in the 13-cis conformation. In conclusion, our findings suggest ultrafast collective motions of aspartic acid residues and functional water molecules in the proximity of the retinal Schiff base as a key facet of this stereoselective and efficient photochemical reaction.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [3];  [4]; ORCiD logo [1];  [5]; ORCiD logo [6];  [1];  [1]; ORCiD logo [7];  [8];  [8]; ORCiD logo [3]; ORCiD logo [3]; ORCiD logo [3];  [1];  [1];  [9];  [1] more »; ORCiD logo [5]; ORCiD logo [10];  [10]; ORCiD logo [11];  [1]; ORCiD logo [9]; ORCiD logo [9];  [3]; ORCiD logo [6]; ORCiD logo [12]; ORCiD logo [8]; ORCiD logo [1] « less
  1. Paul Scherrer Institut (Switzerland). Division of Biology and Chemistry–Laboratory for Biomolecular Research
  2. Paul Scherrer Institut (Switzerland). Division of Biology and Chemistry–Laboratory for Biomolecular Research and Photon Science Division–Swiss Light Source
  3. SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
  4. Paul Scherrer Institut (Switzerland). Science IT
  5. Paul Scherrer Institut (Switzerland). SwissFEL
  6. The Hebrew University of Jerusalem (Israel). Fritz Haber Center for Molecular Dynamics, Institute of Chemistry
  7. Paul Scherrer Institut (Switzerland). SwissFEL and Photon Science Division–Swiss Light Source
  8. University of Gothenburg (Sweden). Department of Chemistry and Molecular Biology
  9. RIKEN SPring-8 Center (Japan); Kyoto University (Japan). Department of Cell Biology, Graduate School of Medicine
  10. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany).Center for Free-Electron Laser Science (CFEL)
  11. Arizona State Univ., Tempe, AZ (United States). Department of Physics
  12. Paul Scherrer Institut (Switzerland). Division of Biology and Chemistry–Laboratory for Biomolecular Research ; ETH Zürich (Switzerland). Department of Biology
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1470908
Grant/Contract Number:  
AC02-76SF00515; 637295; 678169; FP7/2007-2013; FP7-PEOPLE-2011-ITN 317079; 310030_153145; PZ00P3_174169; KAW 2014.0275; SRL10-0036; 2015–00560; 349-2011-6485; 31003A_159558; 142-004
Resource Type:
Accepted Manuscript
Journal Name:
Science
Additional Journal Information:
Journal Volume: 361; Journal Issue: 6398; Journal ID: ISSN 0036-8075
Publisher:
AAAS
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Nogly, Przemyslaw, Weinert, Tobias, James, Daniel, Carbajo, Sergio, Ozerov, Dmitry, Furrer, Antonia, Gashi, Dardan, Borin, Veniamin, Skopintsev, Petr, Jaeger, Kathrin, Nass, Karol, Båth, Petra, Bosman, Robert, Koglin, Jason, Seaberg, Matthew, Lane, Thomas, Kekilli, Demet, Brünle, Steffen, Tanaka, Tomoyuki, Wu, Wenting, Milne, Christopher, White, Thomas, Barty, Anton, Weierstall, Uwe, Panneels, Valerie, Nango, Eriko, Iwata, So, Hunter, Mark, Schapiro, Igor, Schertler, Gebhard, Neutze, Richard, and Standfuss, Jörg. Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser. United States: N. p., 2018. Web. doi:10.1126/science.aat0094.
Nogly, Przemyslaw, Weinert, Tobias, James, Daniel, Carbajo, Sergio, Ozerov, Dmitry, Furrer, Antonia, Gashi, Dardan, Borin, Veniamin, Skopintsev, Petr, Jaeger, Kathrin, Nass, Karol, Båth, Petra, Bosman, Robert, Koglin, Jason, Seaberg, Matthew, Lane, Thomas, Kekilli, Demet, Brünle, Steffen, Tanaka, Tomoyuki, Wu, Wenting, Milne, Christopher, White, Thomas, Barty, Anton, Weierstall, Uwe, Panneels, Valerie, Nango, Eriko, Iwata, So, Hunter, Mark, Schapiro, Igor, Schertler, Gebhard, Neutze, Richard, & Standfuss, Jörg. Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser. United States. https://doi.org/10.1126/science.aat0094
Nogly, Przemyslaw, Weinert, Tobias, James, Daniel, Carbajo, Sergio, Ozerov, Dmitry, Furrer, Antonia, Gashi, Dardan, Borin, Veniamin, Skopintsev, Petr, Jaeger, Kathrin, Nass, Karol, Båth, Petra, Bosman, Robert, Koglin, Jason, Seaberg, Matthew, Lane, Thomas, Kekilli, Demet, Brünle, Steffen, Tanaka, Tomoyuki, Wu, Wenting, Milne, Christopher, White, Thomas, Barty, Anton, Weierstall, Uwe, Panneels, Valerie, Nango, Eriko, Iwata, So, Hunter, Mark, Schapiro, Igor, Schertler, Gebhard, Neutze, Richard, and Standfuss, Jörg. Fri . "Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser". United States. https://doi.org/10.1126/science.aat0094. https://www.osti.gov/servlets/purl/1470908.
@article{osti_1470908,
title = {Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser},
author = {Nogly, Przemyslaw and Weinert, Tobias and James, Daniel and Carbajo, Sergio and Ozerov, Dmitry and Furrer, Antonia and Gashi, Dardan and Borin, Veniamin and Skopintsev, Petr and Jaeger, Kathrin and Nass, Karol and Båth, Petra and Bosman, Robert and Koglin, Jason and Seaberg, Matthew and Lane, Thomas and Kekilli, Demet and Brünle, Steffen and Tanaka, Tomoyuki and Wu, Wenting and Milne, Christopher and White, Thomas and Barty, Anton and Weierstall, Uwe and Panneels, Valerie and Nango, Eriko and Iwata, So and Hunter, Mark and Schapiro, Igor and Schertler, Gebhard and Neutze, Richard and Standfuss, Jörg},
abstractNote = {Ultrafast isomerization of retinal is the primary step in photoresponsive biological functions including vision in humans and ion transport across bacterial membranes. In this study, we used an x-ray laser to study the subpicosecond structural dynamics of retinal isomerization in the light-driven proton pump bacteriorhodopsin. A series of structural snapshots with near-atomic spatial resolution and temporal resolution in the femtosecond regime show how the excited all-trans retinal samples conformational states within the protein binding pocket before passing through a twisted geometry and emerging in the 13-cis conformation. In conclusion, our findings suggest ultrafast collective motions of aspartic acid residues and functional water molecules in the proximity of the retinal Schiff base as a key facet of this stereoselective and efficient photochemical reaction.},
doi = {10.1126/science.aat0094},
journal = {Science},
number = 6398,
volume = 361,
place = {United States},
year = {2018},
month = {7}
}

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