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. Tame

Sam Yong Park, John C.H. Spence, Wenkai Zhang, Marius Schmidt, Weontae Lee, Haiguang Liu

Yonsei University
China Academy of Engineering Physics
Tsinghua University
Beijing Normal University
Arizona State University
University of Wisconsin-Milwaukee
SLAC National Accelerator Laboratory
ARC Centre of Excellence in Advanced Molecular Imaging
Yokohama City University

Research output: Contribution to journal › Article › peer-review

54 Scopus citations

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
State	Published - 30 Mar 2021
Externally published	Yes

Keywords

Light-driven chloride-pumping rhodopsin
Serial femtosecond crystallography
Time-resolved crystallography
X-ray free-electron laser

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10.1073/pnas.2020486118

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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), Article e2020486118. https://doi.org/10.1073/pnas.2020486118

@article{e8d9ffae24044bea99eaff018532889b,

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.",

keywords = "Light-driven chloride-pumping rhodopsin, Serial femtosecond crystallography, Time-resolved crystallography, X-ray free-electron laser",

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",

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",

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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

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.

KW - Light-driven chloride-pumping rhodopsin

KW - Serial femtosecond crystallography

KW - Time-resolved crystallography

KW - X-ray free-electron laser

UR - https://www.scopus.com/pages/publications/85102933338

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

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Keywords

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