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

Przemyslaw Nogly, Tobias Weinert, Daniel James, Sergio Carbajo, Dmitry Ozerov, Antonia Furrer, Dardan Gashi, Veniamin Borin, Petr Skopintsev, Kathrin Jaeger, Karol Nass, Petra Båth, Robert Bosman, Jason Koglin, Matthew Seaberg, Thomas Lane, Demet Kekilli, Steffen Brünle, Tomoyuki Tanaka, Wenting WuChristopher Milne, Thomas White, Anton Barty, Uwe Weierstall, Valerie Panneels, Eriko Nango, So Iwata, Mark Hunter, Igor Schapiro, Gebhard Schertler, Richard Neutze, Jörg Standfuss*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

223 Scopus citations

Abstract

Ultrafast isomerization of retinal is the primary step in photoresponsive biological functions including vision in humans and ion transport across bacterial membranes. 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. 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.

Original languageAmerican English
Article numbereaat0094
JournalScience
Volume361
Issue number6398
DOIs
StatePublished - 13 Jul 2018

Bibliographical note

Funding Information:
We thank the SwissFEL and particularly R. Abela for their constant logistic and financial support in implementing injector-based serial crystallography. We thank F. Dworkowski for help with auxiliary LCP absorption and scattering experiments. We are grateful to the staff at the X06SA beamline at the Swiss Light Source for their assistance in pretesting crystals. Data collection was carried out at the LCLS at the SLAC National Accelerator Laboratory during the LP41 beamtime in June 2017. Use of the LCLS SLAC National Accelerator Laboratory, is supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences under contract no. DE-AC02-76SF00515. T.T., E.N., and S.I. acknowledge support from the X-ray Free Electron Laser Priority Strategy Program (MEXT) and the Platform Project for Supporting Drug Discovery and Life Science Research from the Japan Agency for Medical Research and Development. Th.W. and A.B. acknowledge funding from the Helmholtz Association via Programme Oriented Funds. I.S. has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement 678169 “PhotoMutant”). The work was financially supported by grant FP7-PEOPLE-2011-ITN 317079 NanoMem (to G.S. and R.N.) and Horizon2020 grant XPROBE 637295 (to R.N). We further acknowledge the Swiss National Science Foundation for grants 310030_153145 and 310030B_173335 (to G.S.), PZ00P3_174169 (to P.N.), and 31003A_179351 and 31003A_159558 (to J.S.). P.N. acknowledges support from the European Commission’s Seventh Framework Programme (FP7/2007-2013) under grant agreement no. 290605 (PSI-FELLOW/COFUND). This project has received funding from the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement no. 701647. We acknowledge support from the Data Analysis Service (142-004) project of the Swiss Universities SUC-P2 program. R.N. acknowledges funding from the Swedish Research Council (2015–00560 and 349-2011-6485), the Swedish Foundation for Strategic Research (SRL10-0036), and the Knut and Alice Wallenberg Foundation (KAW 2014.0275). G.S. acknowled es su ort throu h the NCCR MUST/ETH FAST program of the ETH Zürich.

Publisher Copyright:
2017 © The Authors

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