Early-stage dynamics of chloride ion–pumping rhodopsin revealed by a femtosecond X-ray laser

Ji Hye Yun; Xuanxuan Li; Jianing Yue; Jae Hyun Park; Zeyu Jin; Chufeng Li; Hao Hu; Yingchen Shi; Suraj Pandey; Sergio Carbajo; Sébastien Boutet; Mark S. Hunter; Mengning Liang; Raymond G. Sierra; Thomas J. Lane; Liang Zhou; Uwe Weierstall; Nadia A. Zatsepin; Mio Ohki; Jeremy R.H. Tame; Sam Yong Park; John C.H. Spence; Wenkai Zhang; Marius Schmidt; Weontae Lee; Haiguang Liu

doi:10.1073/pnas.2020486118

Early-stage dynamics of chloride ion–pumping rhodopsin revealed by a femtosecond X-ray laser

Ji Hye Yun, Xuanxuan Li, Jianing Yue, Jae Hyun Park, Zeyu Jin, Chufeng Li, Hao Hu, Yingchen Shi, Suraj Pandey, Sergio Carbajo, Sébastien Boutet, Mark S. Hunter, Mengning Liang, Raymond G. Sierra, Thomas J. Lane, Liang Zhou, Uwe Weierstall, Nadia A. Zatsepin, Mio Ohki, Jeremy R.H. TameSam Yong Park, John C.H. Spence, Wenkai Zhang, Marius Schmidt, Weontae Lee, Haiguang Liu

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Abstract

Chloride ion–pumping rhodopsin (ClR) in some marine bacteria utilizes light energy to actively transport Cl⁻ into cells. How the ClR initiates the transport is elusive. Here, we show the dynamics of ion transport observed with time-resolved serial femtosecond (fs) crystallography using the Linac Coherent Light Source. X-ray pulses captured structural changes in ClR upon flash illumination with a 550 nm fs-pumping laser. High-resolution structures for five time points (dark to 100 ps after flashing) reveal complex and coordinated dynamics comprising retinal isomerization, water molecule rearrangement, and conformational changes of various residues. Combining data from time-resolved spectroscopy experiments and molecular dynamics simulations, this study reveals that the chloride ion close to the Schiff base undergoes a dissociation–diffusion process upon light-triggered retinal isomerization.

Original language	English
Article number	e2020486118
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	118
Issue number	13
DOIs	https://doi.org/10.1073/pnas.2020486118
Publication status	Published - 2021 Mar 30

Bibliographical note

Funding Information:
ACKNOWLEDGMENTS. The experiment was conducted at the LCLS, SLAC National Accelerator Laboratory, supported by the US Department of Energy, Office of Science, and Office of Basic Energy Sciences under Contract No. DE-AC02-76SF00515. We would like to acknowledge all members of the PAL-XFEL with the support of Pohang Accelerator Laboratory, Korea. National Natural Science Foundation of China (Grant Nos. 31971136, 11575021, and U1930402 to H.L.; Grant Nos. 21773012 and U2032112 to W.Z.); National Research Foundation of Korea (Grant Nos. NRF-2019M3E5D6063903, 2017M3A9F6029753, and 2018K2A9A2A06024227 to W.L.; and NRF-2016R1A6A3A04010213 to J.-H.Y.); The STC Program of the NSF through BioXFEL under Agreement No. 1231306 (U.W., N.A.Z., J.C.H.S., and M.S.); and NSF ABI Innovations Award No. 1565180 (C.L., U.W., N.A.Z., and J.C.H.S.). NSF Grant No. 2030466 to M.S. Parts of the sample injector used at LCLS for this research were funded by the NIH, P41GM103393, formerly P41RR001209. J.R.H.T. received funding from Open-Eye Scientific Software.

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© 2021 National Academy of Sciences. All rights reserved.

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Yun, J. H., Li, X., Yue, J., Park, J. H., Jin, Z., Li, C., Hu, H., Shi, Y., Pandey, S., Carbajo, S., Boutet, S., Hunter, M. S., Liang, M., Sierra, R. G., Lane, T. J., Zhou, L., Weierstall, U., Zatsepin, N. A., Ohki, M., ... Liu, H. (2021). Early-stage dynamics of chloride ion–pumping rhodopsin revealed by a femtosecond X-ray laser. Proceedings of the National Academy of Sciences of the United States of America, 118(13), [e2020486118]. https://doi.org/10.1073/pnas.2020486118

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title = "Early-stage dynamics of chloride ion–pumping rhodopsin revealed by a femtosecond X-ray laser",

abstract = "Chloride ion–pumping rhodopsin (ClR) in some marine bacteria utilizes light energy to actively transport Cl− into cells. How the ClR initiates the transport is elusive. Here, we show the dynamics of ion transport observed with time-resolved serial femtosecond (fs) crystallography using the Linac Coherent Light Source. X-ray pulses captured structural changes in ClR upon flash illumination with a 550 nm fs-pumping laser. High-resolution structures for five time points (dark to 100 ps after flashing) reveal complex and coordinated dynamics comprising retinal isomerization, water molecule rearrangement, and conformational changes of various residues. Combining data from time-resolved spectroscopy experiments and molecular dynamics simulations, this study reveals that the chloride ion close to the Schiff base undergoes a dissociation–diffusion process upon light-triggered retinal isomerization.",

author = "Yun, {Ji Hye} and Xuanxuan Li and Jianing Yue and Park, {Jae Hyun} and Zeyu Jin and Chufeng Li and Hao Hu and Yingchen Shi and Suraj Pandey and Sergio Carbajo and S{\'e}bastien Boutet and Hunter, {Mark S.} and Mengning Liang and Sierra, {Raymond G.} and Lane, {Thomas J.} and Liang Zhou and Uwe Weierstall and Zatsepin, {Nadia A.} and Mio Ohki and Tame, {Jeremy R.H.} and Park, {Sam Yong} and Spence, {John C.H.} and Wenkai Zhang and Marius Schmidt and Weontae Lee and Haiguang Liu",

note = "Funding Information: ACKNOWLEDGMENTS. The experiment was conducted at the LCLS, SLAC National Accelerator Laboratory, supported by the US Department of Energy, Office of Science, and Office of Basic Energy Sciences under Contract No. DE-AC02-76SF00515. We would like to acknowledge all members of the PAL-XFEL with the support of Pohang Accelerator Laboratory, Korea. National Natural Science Foundation of China (Grant Nos. 31971136, 11575021, and U1930402 to H.L.; Grant Nos. 21773012 and U2032112 to W.Z.); National Research Foundation of Korea (Grant Nos. NRF-2019M3E5D6063903, 2017M3A9F6029753, and 2018K2A9A2A06024227 to W.L.; and NRF-2016R1A6A3A04010213 to J.-H.Y.); The STC Program of the NSF through BioXFEL under Agreement No. 1231306 (U.W., N.A.Z., J.C.H.S., and M.S.); and NSF ABI Innovations Award No. 1565180 (C.L., U.W., N.A.Z., and J.C.H.S.). NSF Grant No. 2030466 to M.S. Parts of the sample injector used at LCLS for this research were funded by the NIH, P41GM103393, formerly P41RR001209. J.R.H.T. received funding from Open-Eye Scientific Software. Publisher Copyright: {\textcopyright} 2021 National Academy of Sciences. All rights reserved.",

year = "2021",

month = mar,

day = "30",

doi = "10.1073/pnas.2020486118",

language = "English",

volume = "118",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "National Academy of Sciences",

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}

Yun, JH, Li, X, Yue, J, Park, JH, Jin, Z, Li, C, Hu, H, Shi, Y, Pandey, S, Carbajo, S, Boutet, S, Hunter, MS, Liang, M, Sierra, RG, Lane, TJ, Zhou, L, Weierstall, U, Zatsepin, NA, Ohki, M, Tame, JRH, Park, SY, Spence, JCH, Zhang, W, Schmidt, M, Lee, W & Liu, H 2021, 'Early-stage dynamics of chloride ion–pumping rhodopsin revealed by a femtosecond X-ray laser', Proceedings of the National Academy of Sciences of the United States of America, vol. 118, no. 13, e2020486118. https://doi.org/10.1073/pnas.2020486118

TY - JOUR

T1 - Early-stage dynamics of chloride ion–pumping rhodopsin revealed by a femtosecond X-ray laser

AU - Yun, Ji Hye

AU - Li, Xuanxuan

AU - Yue, Jianing

AU - Park, Jae Hyun

AU - Jin, Zeyu

AU - Li, Chufeng

AU - Hu, Hao

AU - Shi, Yingchen

AU - Pandey, Suraj

AU - Carbajo, Sergio

AU - Boutet, Sébastien

AU - Hunter, Mark S.

AU - Liang, Mengning

AU - Sierra, Raymond G.

AU - Lane, Thomas J.

AU - Zhou, Liang

AU - Weierstall, Uwe

AU - Zatsepin, Nadia A.

AU - Ohki, Mio

AU - Tame, Jeremy R.H.

AU - Park, Sam Yong

AU - Spence, John C.H.

AU - Zhang, Wenkai

AU - Schmidt, Marius

AU - Lee, Weontae

AU - Liu, Haiguang

N1 - Funding Information: ACKNOWLEDGMENTS. The experiment was conducted at the LCLS, SLAC National Accelerator Laboratory, supported by the US Department of Energy, Office of Science, and Office of Basic Energy Sciences under Contract No. DE-AC02-76SF00515. We would like to acknowledge all members of the PAL-XFEL with the support of Pohang Accelerator Laboratory, Korea. National Natural Science Foundation of China (Grant Nos. 31971136, 11575021, and U1930402 to H.L.; Grant Nos. 21773012 and U2032112 to W.Z.); National Research Foundation of Korea (Grant Nos. NRF-2019M3E5D6063903, 2017M3A9F6029753, and 2018K2A9A2A06024227 to W.L.; and NRF-2016R1A6A3A04010213 to J.-H.Y.); The STC Program of the NSF through BioXFEL under Agreement No. 1231306 (U.W., N.A.Z., J.C.H.S., and M.S.); and NSF ABI Innovations Award No. 1565180 (C.L., U.W., N.A.Z., and J.C.H.S.). NSF Grant No. 2030466 to M.S. Parts of the sample injector used at LCLS for this research were funded by the NIH, P41GM103393, formerly P41RR001209. J.R.H.T. received funding from Open-Eye Scientific Software. Publisher Copyright: © 2021 National Academy of Sciences. All rights reserved.

PY - 2021/3/30

Y1 - 2021/3/30

N2 - Chloride ion–pumping rhodopsin (ClR) in some marine bacteria utilizes light energy to actively transport Cl− into cells. How the ClR initiates the transport is elusive. Here, we show the dynamics of ion transport observed with time-resolved serial femtosecond (fs) crystallography using the Linac Coherent Light Source. X-ray pulses captured structural changes in ClR upon flash illumination with a 550 nm fs-pumping laser. High-resolution structures for five time points (dark to 100 ps after flashing) reveal complex and coordinated dynamics comprising retinal isomerization, water molecule rearrangement, and conformational changes of various residues. Combining data from time-resolved spectroscopy experiments and molecular dynamics simulations, this study reveals that the chloride ion close to the Schiff base undergoes a dissociation–diffusion process upon light-triggered retinal isomerization.

AB - Chloride ion–pumping rhodopsin (ClR) in some marine bacteria utilizes light energy to actively transport Cl− into cells. How the ClR initiates the transport is elusive. Here, we show the dynamics of ion transport observed with time-resolved serial femtosecond (fs) crystallography using the Linac Coherent Light Source. X-ray pulses captured structural changes in ClR upon flash illumination with a 550 nm fs-pumping laser. High-resolution structures for five time points (dark to 100 ps after flashing) reveal complex and coordinated dynamics comprising retinal isomerization, water molecule rearrangement, and conformational changes of various residues. Combining data from time-resolved spectroscopy experiments and molecular dynamics simulations, this study reveals that the chloride ion close to the Schiff base undergoes a dissociation–diffusion process upon light-triggered retinal isomerization.

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UR - http://www.scopus.com/inward/citedby.url?scp=85102933338&partnerID=8YFLogxK

U2 - 10.1073/pnas.2020486118

DO - 10.1073/pnas.2020486118

M3 - Article

C2 - 33753488

AN - SCOPUS:85102933338

SN - 0027-8424

VL - 118

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 13

M1 - e2020486118

ER -

Early-stage dynamics of chloride ion–pumping rhodopsin revealed by a femtosecond X-ray laser

Abstract

Bibliographical note

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UN SDGs

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