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Structural insights into light-driven anion pumping in cyanobacteria

Author

Listed:
  • R. Astashkin

    (Univ. Grenoble Alpes, CEA, CNRS, Institut de Biologie Structurale (IBS))

  • K. Kovalev

    (European Molecular Biology Laboratory, Hamburg unit c/o DESY)

  • S. Bukhdruker

    (European Synchrotron Radiation Facility Grenoble
    Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich)

  • S. Vaganova

    (Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich)

  • A. Kuzmin

    (Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology)

  • A. Alekseev

    (Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology)

  • T. Balandin

    (Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich)

  • D. Zabelskii

    (European XFEL GmbH)

  • I. Gushchin

    (Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology)

  • A. Royant

    (Univ. Grenoble Alpes, CEA, CNRS, Institut de Biologie Structurale (IBS)
    European Synchrotron Radiation Facility Grenoble)

  • D. Volkov

    (Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich)

  • G. Bourenkov

    (European Molecular Biology Laboratory, Hamburg unit c/o DESY)

  • E. Koonin

    (National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health)

  • M. Engelhard

    (Max Planck Institute of Molecular Physiology)

  • E. Bamberg

    (Max Planck Institute of Biophysics)

  • V. Gordeliy

    (Univ. Grenoble Alpes, CEA, CNRS, Institut de Biologie Structurale (IBS)
    Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich)

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.

Suggested Citation

  • 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. Bamb, 2022. "Structural insights into light-driven anion pumping in cyanobacteria," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34019-9
    DOI: 10.1038/s41467-022-34019-9
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    References listed on IDEAS

    as
    1. Kuglae Kim & Soon-Kyeong Kwon & Sung-Hoon Jun & Jeong Seok Cha & Hoyoung Kim & Weontae Lee & Jihyun F. Kim & Hyun-Soo Cho, 2016. "Crystal structure and functional characterization of a light-driven chloride pump having an NTQ motif," Nature Communications, Nature, vol. 7(1), pages 1-10, November.
    2. Hideaki E. Kato & Motoshi Kamiya & Seiya Sugo & Jumpei Ito & Reiya Taniguchi & Ayaka Orito & Kunio Hirata & Ayumu Inutsuka & Akihiro Yamanaka & Andrés D. Maturana & Ryuichiro Ishitani & Yuki Sudo & Sh, 2015. "Atomistic design of microbial opsin-based blue-shifted optogenetics tools," Nature Communications, Nature, vol. 6(1), pages 1-10, November.
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