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

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

42 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 (US)
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 - Mar 30 2021

Keywords

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

ASJC Scopus subject areas

General

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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

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

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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.",

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

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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

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

Abstract

Keywords

ASJC Scopus subject areas

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1 ps Structure of Chloride ion pumping rhodopsin (ClR) with NTQ motif

Structure of Chloride ion pumping rhodopsin (ClR) with NTQ motif 100 ps after light activation (2.63mJ/mm2)

Structure of Chloride ion pumping rhodopsin (ClR) with NTQ motif 100 ps after light activation (0.17mJ/mm2)

Cite this

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

Abstract

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Datasets

1 ps Structure of Chloride ion pumping rhodopsin (ClR) with NTQ motif

Structure of Chloride ion pumping rhodopsin (ClR) with NTQ motif 100 ps after light activation (2.63mJ/mm2)

Structure of Chloride ion pumping rhodopsin (ClR) with NTQ motif 100 ps after light activation (0.17mJ/mm2)

Cite this