Dynamics and mechanism of a light-driven chloride pump

Sandra Mous; Guillaume Gotthard; David Ehrenberg; Saumik Sen; Tobias Weinert; Philip J.M. Johnson; Daniel James; Karol Nass; Antonia Furrer; Demet Kekilli; Pikyee Ma; Steffen Brünle; Cecilia Maria Casadei; Isabelle Martiel; Florian Dworkowski; Dardan Gashi; Petr Skopintsev; Maximilian Wranik; Gregor Knopp; Ezequiel Panepucci; Valerie Panneels; Claudio Cirelli; Dmitry Ozerov; Gebhard F.X. Schertler; Meitian Wang; Chris Milne; Joerg Standfuss; Igor Schapiro; Joachim Heberle; Przemyslaw Nogly

doi:10.1126/science.abj6663

Dynamics and mechanism of a light-driven chloride pump

Sandra Mous, Guillaume Gotthard, David Ehrenberg, Saumik Sen, Tobias Weinert, Philip J.M. Johnson, Daniel James, Karol Nass, Antonia Furrer, Demet Kekilli, Pikyee Ma, Steffen Brünle, Cecilia Maria Casadei, Isabelle Martiel, Florian Dworkowski, Dardan Gashi, Petr Skopintsev, Maximilian Wranik, Gregor Knopp, Ezequiel PanepucciValerie Panneels, Claudio Cirelli, Dmitry Ozerov, Gebhard F.X. Schertler, Meitian Wang, Chris Milne, Joerg Standfuss, Igor Schapiro, Joachim Heberle, Przemyslaw Nogly^*

^*Corresponding author for this work

Institute of Chemistry

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

53 Scopus citations

Abstract

Chloride transport by microbial rhodopsins is an essential process for which molecular details such as the mechanisms that convert light energy to drive ion pumping and ensure the unidirectionality of the transport have remained elusive. We combined time-resolved serial crystallography with time-resolved spectroscopy and multiscale simulations to elucidate the molecular mechanism of a chloride-pumping rhodopsin and the structural dynamics throughout the transport cycle. We traced transient anion-binding sites, obtained evidence for how light energy is used in the pumping mechanism, and identified steric and electrostatic molecular gates ensuring unidirectional transport. An interaction with the π-electron system of the retinal supports transient chloride ion binding across a major bottleneck in the transport pathway. These results allow us to propose key mechanistic features enabling finely controlled chloride transport across the cell membrane in this light-powered chloride ion pump.

Original language	English
Pages (from-to)	845-851
Number of pages	7
Journal	Science
Volume	375
Issue number	6583
DOIs	https://doi.org/10.1126/science.abj6663
State	Published - 25 Feb 2022

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© 2022 American Association for the Advancement of Science. All rights reserved.

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Mous, S., Gotthard, G., Ehrenberg, D., Sen, S., Weinert, T., Johnson, P. J. M., James, D., Nass, K., Furrer, A., Kekilli, D., Ma, P., Brünle, S., Maria Casadei, C., Martiel, I., Dworkowski, F., Gashi, D., Skopintsev, P., Wranik, M., Knopp, G., ... Nogly, P. (2022). Dynamics and mechanism of a light-driven chloride pump. Science, 375(6583), 845-851. https://doi.org/10.1126/science.abj6663

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title = "Dynamics and mechanism of a light-driven chloride pump",

abstract = "Chloride transport by microbial rhodopsins is an essential process for which molecular details such as the mechanisms that convert light energy to drive ion pumping and ensure the unidirectionality of the transport have remained elusive. We combined time-resolved serial crystallography with time-resolved spectroscopy and multiscale simulations to elucidate the molecular mechanism of a chloride-pumping rhodopsin and the structural dynamics throughout the transport cycle. We traced transient anion-binding sites, obtained evidence for how light energy is used in the pumping mechanism, and identified steric and electrostatic molecular gates ensuring unidirectional transport. An interaction with the π-electron system of the retinal supports transient chloride ion binding across a major bottleneck in the transport pathway. These results allow us to propose key mechanistic features enabling finely controlled chloride transport across the cell membrane in this light-powered chloride ion pump.",

author = "Sandra Mous and Guillaume Gotthard and David Ehrenberg and Saumik Sen and Tobias Weinert and Johnson, {Philip J.M.} and Daniel James and Karol Nass and Antonia Furrer and Demet Kekilli and Pikyee Ma and Steffen Br{\"u}nle and {Maria Casadei}, Cecilia and Isabelle Martiel and Florian Dworkowski and Dardan Gashi and Petr Skopintsev and Maximilian Wranik and Gregor Knopp and Ezequiel Panepucci and Valerie Panneels and Claudio Cirelli and Dmitry Ozerov and Schertler, {Gebhard F.X.} and Meitian Wang and Chris Milne and Joerg Standfuss and Igor Schapiro and Joachim Heberle and Przemyslaw Nogly",

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Mous, S, Gotthard, G, Ehrenberg, D, Sen, S, Weinert, T, Johnson, PJM, James, D, Nass, K, Furrer, A, Kekilli, D, Ma, P, Brünle, S, Maria Casadei, C, Martiel, I, Dworkowski, F, Gashi, D, Skopintsev, P, Wranik, M, Knopp, G, Panepucci, E, Panneels, V, Cirelli, C, Ozerov, D, Schertler, GFX, Wang, M, Milne, C, Standfuss, J, Schapiro, I, Heberle, J & Nogly, P 2022, 'Dynamics and mechanism of a light-driven chloride pump', Science, vol. 375, no. 6583, pp. 845-851. https://doi.org/10.1126/science.abj6663

TY - JOUR

T1 - Dynamics and mechanism of a light-driven chloride pump

AU - Mous, Sandra

AU - Gotthard, Guillaume

AU - Ehrenberg, David

AU - Sen, Saumik

AU - Weinert, Tobias

AU - Johnson, Philip J.M.

AU - James, Daniel

AU - Nass, Karol

AU - Furrer, Antonia

AU - Kekilli, Demet

AU - Ma, Pikyee

AU - Brünle, Steffen

AU - Maria Casadei, Cecilia

AU - Martiel, Isabelle

AU - Dworkowski, Florian

AU - Gashi, Dardan

AU - Skopintsev, Petr

AU - Wranik, Maximilian

AU - Knopp, Gregor

AU - Panepucci, Ezequiel

AU - Panneels, Valerie

AU - Cirelli, Claudio

AU - Ozerov, Dmitry

AU - Schertler, Gebhard F.X.

AU - Wang, Meitian

AU - Milne, Chris

AU - Standfuss, Joerg

AU - Schapiro, Igor

AU - Heberle, Joachim

AU - Nogly, Przemyslaw

PY - 2022/2/25

Y1 - 2022/2/25

N2 - Chloride transport by microbial rhodopsins is an essential process for which molecular details such as the mechanisms that convert light energy to drive ion pumping and ensure the unidirectionality of the transport have remained elusive. We combined time-resolved serial crystallography with time-resolved spectroscopy and multiscale simulations to elucidate the molecular mechanism of a chloride-pumping rhodopsin and the structural dynamics throughout the transport cycle. We traced transient anion-binding sites, obtained evidence for how light energy is used in the pumping mechanism, and identified steric and electrostatic molecular gates ensuring unidirectional transport. An interaction with the π-electron system of the retinal supports transient chloride ion binding across a major bottleneck in the transport pathway. These results allow us to propose key mechanistic features enabling finely controlled chloride transport across the cell membrane in this light-powered chloride ion pump.

AB - Chloride transport by microbial rhodopsins is an essential process for which molecular details such as the mechanisms that convert light energy to drive ion pumping and ensure the unidirectionality of the transport have remained elusive. We combined time-resolved serial crystallography with time-resolved spectroscopy and multiscale simulations to elucidate the molecular mechanism of a chloride-pumping rhodopsin and the structural dynamics throughout the transport cycle. We traced transient anion-binding sites, obtained evidence for how light energy is used in the pumping mechanism, and identified steric and electrostatic molecular gates ensuring unidirectional transport. An interaction with the π-electron system of the retinal supports transient chloride ion binding across a major bottleneck in the transport pathway. These results allow us to propose key mechanistic features enabling finely controlled chloride transport across the cell membrane in this light-powered chloride ion pump.

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DO - 10.1126/science.abj6663

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C2 - 35113649

AN - SCOPUS:85125289281

SN - 0036-8075

VL - 375

SP - 845

EP - 851

JO - Science

JF - Science

IS - 6583

ER -

Dynamics and mechanism of a light-driven chloride pump

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