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 Wu; Christopher Milne; Thomas White; Anton Barty; Uwe Weierstall; Valerie Panneels; Eriko Nango; So Iwata; Mark Hunter; Igor Schapiro; Gebhard Schertler; Richard Neutze; Jörg Standfuss

doi:10.1126/science.aat0094

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

Institute of Chemistry

Research output: Contribution to journal › Article › peer-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 language	American English
Article number	eaat0094
Journal	Science
Volume	361
Issue number	6398
DOIs	https://doi.org/10.1126/science.aat0094
State	Published - 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

Access to Document

10.1126/science.aat0094

Cite this

Nogly, P., Weinert, T., James, D., Carbajo, S., Ozerov, D., Furrer, A., Gashi, D., Borin, V., Skopintsev, P., Jaeger, K., Nass, K., Båth, P., Bosman, R., Koglin, J., Seaberg, M., Lane, T., Kekilli, D., Brünle, S., Tanaka, T., ... Standfuss, J. (2018). Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser. Science, 361(6398), Article eaat0094. https://doi.org/10.1126/science.aat0094

@article{ead81e592844486c86344862f5dc3b7c,

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. 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.",

author = "Przemyslaw Nogly and Tobias Weinert and Daniel James and Sergio Carbajo and Dmitry Ozerov and Antonia Furrer and Dardan Gashi and Veniamin Borin and Petr Skopintsev and Kathrin Jaeger and Karol Nass and Petra B{\aa}th and Robert Bosman and Jason Koglin and Matthew Seaberg and Thomas Lane and Demet Kekilli and Steffen Br{\"u}nle and Tomoyuki Tanaka and Wenting Wu and Christopher Milne and Thomas White and Anton Barty and Uwe Weierstall and Valerie Panneels and Eriko Nango and So Iwata and Mark Hunter and Igor Schapiro and Gebhard Schertler and Richard Neutze and J{\"o}rg Standfuss",

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{\textquoteright}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{\textquoteright}s Seventh Framework Programme (FP7/2007-2013) under grant agreement no. 290605 (PSI-FELLOW/COFUND). This project has received funding from the European Union{\textquoteright}s Horizon 2020 research and innovation program under the Marie Sk{\l}odowska-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 Z{\"u}rich. Publisher Copyright: 2017 {\textcopyright} The Authors",

year = "2018",

month = jul,

day = "13",

doi = "10.1126/science.aat0094",

language = "American English",

volume = "361",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

number = "6398",

}

Nogly, P, Weinert, T, James, D, Carbajo, S, Ozerov, D, Furrer, A, Gashi, D, Borin, V, Skopintsev, P, Jaeger, K, Nass, K, Båth, P, Bosman, R, Koglin, J, Seaberg, M, Lane, T, Kekilli, D, Brünle, S, Tanaka, T, Wu, W, Milne, C, White, T, Barty, A, Weierstall, U, Panneels, V, Nango, E, Iwata, S, Hunter, M, Schapiro, I, Schertler, G, Neutze, R & Standfuss, J 2018, 'Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser', Science, vol. 361, no. 6398, eaat0094. https://doi.org/10.1126/science.aat0094

TY - JOUR

T1 - Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser

AU - Nogly, Przemyslaw

AU - Weinert, Tobias

AU - James, Daniel

AU - Carbajo, Sergio

AU - Ozerov, Dmitry

AU - Furrer, Antonia

AU - Gashi, Dardan

AU - Borin, Veniamin

AU - Skopintsev, Petr

AU - Jaeger, Kathrin

AU - Nass, Karol

AU - Båth, Petra

AU - Bosman, Robert

AU - Koglin, Jason

AU - Seaberg, Matthew

AU - Lane, Thomas

AU - Kekilli, Demet

AU - Brünle, Steffen

AU - Tanaka, Tomoyuki

AU - Wu, Wenting

AU - Milne, Christopher

AU - White, Thomas

AU - Barty, Anton

AU - Weierstall, Uwe

AU - Panneels, Valerie

AU - Nango, Eriko

AU - Iwata, So

AU - Hunter, Mark

AU - Schapiro, Igor

AU - Schertler, Gebhard

AU - Neutze, Richard

AU - Standfuss, Jörg

N1 - 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

PY - 2018/7/13

Y1 - 2018/7/13

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85048626677&partnerID=8YFLogxK

U2 - 10.1126/science.aat0094

DO - 10.1126/science.aat0094

M3 - Article

C2 - 29903883

AN - SCOPUS:85048626677

SN - 0036-8075

VL - 361

JO - Science

JF - Science

IS - 6398

M1 - eaat0094

ER -

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

Abstract

Bibliographical note

Access to Document

Other files and links

Fingerprint

Cite this