Structural insights into light-driven anion pumping in cyanobacteria

R. Astashkin; K. Kovalev; S. Bukhdruker; S. Vaganova; A. Kuzmin; A. Alekseev; T. Balandin; D. Zabelskii; I. Gushchin; A. Royant; D. Volkov; G. Bourenkov; E. Koonin; M. Engelhard; E. Bamberg; V. Gordeliy

doi:10.1038/s41467-022-34019-9

Structural insights into light-driven anion pumping in cyanobacteria

R. Astashkin, K. Kovalev, S. Bukhdruker, S. Vaganova, A. Kuzmin, A. Alekseev, T. Balandin, D. Zabelskii, I. Gushchin, A. Royant, D. Volkov, G. Bourenkov, E. Koonin, M. Engelhard, E. Bamberg, V. Gordeliy

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Transmembrane ion transport is a key process in living cells. Active transport of ions is carried out by various ion transporters including microbial rhodopsins (MRs). MRs perform diverse functions such as active and passive ion transport, photo-sensing, and others. In particular, MRs can pump various monovalent ions like Na+, K+, Cl−, I−, NO3−. The only characterized MR proposed to pump sulfate in addition to halides belongs to the cyanobacterium Synechocystis sp. PCC 7509 and is named Synechocystis halorhodopsin (SyHR). The structural study of SyHR may help to understand what makes an MR pump divalent ions. Here we present the crystal structure of SyHR in the ground state, the structure of its sulfate-bound form as well as two photoreaction intermediates, the K and O states. These data reveal the molecular origin of the unique properties of the protein (exceptionally strong chloride binding and proposed pumping of divalent anions) and sheds light on the mechanism of anion release and uptake in cyanobacterial halorhodopsins. The unique properties of SyHR highlight its potential as an optogenetics tool and may help engineer different types of anion pumps with applications in optogenetics.

Original language	English
Article number	6460
Journal	Nature Communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-34019-9
Publication status	Published - 1 Dec 2022
Externally published	Yes

Funding

We acknowledge the Structural Biology Group of the European Synchrotron Radiation Facility and the European Molecular Biology Laboratory (EMBL) unit in Hamburg at Deutsche Elektronen-Synchrotron (DESY) for granting access to the synchrotron beamlines. Funding: This work was supported by the common program of Agence Nationale de la Recherche (ANR), France and Deutsche Forschungsgemeinschaft, Germany (ANR-15-CE11-0029-02), as well as by funding from Frankfurt: Cluster of Excellence Frankfurt Macromolecular Complexes (to E.B.), by the Max Planck Society (to E.B.) and by the Commissariat \u00E0 l\u2019Energie Atomique et aux Energies Alternatives (Institut de Biologie Structurale)\u2013Helmholtz-Gemeinschaft Deutscher Forschungszentren (Forschungszentrum J\u00FClich) Special Terms and Conditions 5.1 specific agreement. A.K. was supported by the Ministry of Science and Higher Education of the Russian Federation (agreement 075-03-2022-107, project FSMG-2021-0002). A.A. was supported by the Ministry of Science and Higher Education of the Russian Federation (agreement 075-01645-22-06, project 720000\u2009F.99.1.B\u041785AV67000). Structure analysis was supported by the Russian Science Foundation, grant number 21-64-00018 (to I.G.). This work used the platforms of the Grenoble Instruct Centre (ISBG; UMS 3518 CNRS-CEA-UJF-EMBL) with support from the French Infrastructure for Integrated Structural Biology (ANR-10-INSB-05-02) and GRAL (ANR-10-LABX-49-01) within the Grenoble Partnership for Structural Biology.

Funders	Funder number
Max-Planck-Gesellschaft
Helmholtz-Gemeinschaft
Commissariat à l'Énergie Atomique et aux Énergies Alternatives
Cluster of Excellence Frankfurt Macromolecular Complexes
Grenoble Instruct centre
European Molecular Biology Laboratory
Institut de Biologie Structurale
European Synchrotron Radiation Facility
Ministry of Education and Science of the Russian Federation	075-01645-22-06, 075-03-2022-107, 720000 F.99.1, BЗ85AV67000, FSMG-2021-0002
Russian Science Foundation	21-64-00018
ISBG	UMS 3518 CNRS-CEA-UJF-EMBL
Agence Nationale de la Recherche	ANR-15-CE11-0029
French Infrastructure for Integrated Structural Biology	ANR-10-LABX-49-01, ANR-10-INSB-05-02
Deutsche Forschungsgemeinschaft	ANR-15-CE11-0029-02

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Astashkin, R., Kovalev, K., Bukhdruker, S., Vaganova, S., Kuzmin, A., Alekseev, A., Balandin, T., Zabelskii, D., Gushchin, I., Royant, A., Volkov, D., Bourenkov, G., Koonin, E., Engelhard, M., Bamberg, E., & Gordeliy, V. (2022). Structural insights into light-driven anion pumping in cyanobacteria. Nature Communications, 13(1), Article 6460. https://doi.org/10.1038/s41467-022-34019-9

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abstract = "Transmembrane ion transport is a key process in living cells. Active transport of ions is carried out by various ion transporters including microbial rhodopsins (MRs). MRs perform diverse functions such as active and passive ion transport, photo-sensing, and others. In particular, MRs can pump various monovalent ions like Na+, K+, Cl−, I−, NO3−. The only characterized MR proposed to pump sulfate in addition to halides belongs to the cyanobacterium Synechocystis sp. PCC 7509 and is named Synechocystis halorhodopsin (SyHR). The structural study of SyHR may help to understand what makes an MR pump divalent ions. Here we present the crystal structure of SyHR in the ground state, the structure of its sulfate-bound form as well as two photoreaction intermediates, the K and O states. These data reveal the molecular origin of the unique properties of the protein (exceptionally strong chloride binding and proposed pumping of divalent anions) and sheds light on the mechanism of anion release and uptake in cyanobacterial halorhodopsins. The unique properties of SyHR highlight its potential as an optogenetics tool and may help engineer different types of anion pumps with applications in optogenetics.",

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AU - Alekseev, A.

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AU - Volkov, D.

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Structural insights into light-driven anion pumping in cyanobacteria

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