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Structure-based insights into evolution of rhodopsins

Communications Biology, vol. 4, pp. 821

Abstract

Rhodopsins, most of which are proton pumps generating transmembrane electrochemical proton gradients, span all three domains of life, are abundant in the biosphere, and could play a crucial role in the early evolution of life on earth. Whereas archaeal and bacterial proton pumps are among the best structurally characterized proteins, rhodopsins from unicellular eukaryotes have not been well characterized. To fill this gap in the current understanding of the proton pumps and to gain insight into the evolution of rhodopsins using a structure-based approach, we performed a structural and functional analysis of the light-driven proton pump LR (Mac) from the pathogenic fungus Leptosphaeria maculans. The first high-resolution structure of fungi rhodopsin and its functional properties reveal the striking similarity of its membrane part to archaeal but not to bacterial rhodopsins. We show that an unusually long N-terminal region stabilizes the protein through direct interaction with its extracellular loop (ECL2). We compare to our knowledge all available structures and sequences of outward light-driven proton pumps and show that eukaryotic and archaeal proton pumps, most likely, share a common ancestor.

Authors 21

  1. Moscow Institute of Physics and Technology · Forschungszentrum Jülich

    Affiliation as printed

    Institute of Biological Information Processing (IBI-7: Structural Biochemistry), ForschungszentrumJülich, Jülich, Germany

    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich, Jülich, Germany

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

  2. Forschungszentrum Jülich

    Affiliation as printed

    Institute of Biological Information Processing (IBI-7: Structural Biochemistry), ForschungszentrumJülich, Jülich, Germany

    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich, Jülich, Germany

  3. Moscow Institute of Physics and Technology · RWTH Aachen University

    Affiliation as printed

    Institute of Crystallography, University of Aachen (RWTH), Aachen, Germany

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

  4. Centre National de la Recherche Scientifique · Moscow Institute of Physics and Technology · Commissariat à l'Énergie Atomique et aux Énergies Alternatives · Institut de Biologie Structurale · European Molecular Biology Laboratory · Université Grenoble Alpes

    Affiliation as printed

    European Molecular Biology Laboratory, Hamburg unit c/o DESY, Hamburg, Germany

    Institut de Biologie Structurale (IBS), Université Grenoble Alpes-CEA-CNRS, Grenoble, France

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

  5. Forschungszentrum Jülich

    Affiliation as printed

    Institute of Biological Information Processing (IBI-7: Structural Biochemistry), ForschungszentrumJülich, Jülich, Germany

    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich, Jülich, Germany

  6. Moscow Institute of Physics and Technology · Joint Institute for Nuclear Research · Institute for Safety Problems of Nuclear Power Plants

    Affiliation as printed

    Institute for Safety Problems of Nuclear Power Plants, NAS of Ukraine, Kyiv, Ukraine

    Joint Institute for Nuclear Research, Dubna, Russia

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

  7. Centre National de la Recherche Scientifique · Moscow Institute of Physics and Technology · Commissariat à l'Énergie Atomique et aux Énergies Alternatives · Institut de Biologie Structurale · Université Grenoble Alpes

    Affiliation as printed

    Institut de Biologie Structurale (IBS), Université Grenoble Alpes-CEA-CNRS, Grenoble, France

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

  8. Centre National de la Recherche Scientifique · Moscow Institute of Physics and Technology · Forschungszentrum Jülich · Commissariat à l'Énergie Atomique et aux Énergies Alternatives · Institut de Biologie Structurale · RWTH Aachen University · Université Grenoble Alpes

    Affiliation as printed

    Institut de Biologie Structurale (IBS), Université Grenoble Alpes-CEA-CNRS, Grenoble, France

    Institute of Biological Information Processing (IBI-7: Structural Biochemistry), ForschungszentrumJülich, Jülich, Germany

    Institute of Crystallography, University of Aachen (RWTH), Aachen, Germany

    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich, Jülich, Germany

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

  9. Moscow Institute of Physics and Technology · Forschungszentrum Jülich · RWTH Aachen University

    Affiliation as printed

    Institute of Biological Information Processing (IBI-7: Structural Biochemistry), ForschungszentrumJülich, Jülich, Germany

    Institute of Crystallography, University of Aachen (RWTH), Aachen, Germany

    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich, Jülich, Germany

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

  10. Forschungszentrum Jülich · European Molecular Biology Laboratory

    Affiliation as printed

    European Molecular Biology Laboratory, Hamburg Unit, Notkestrasse 25a, Hamburg, Germany

    Institute of Biological Information Processing (IBI-7: Structural Biochemistry), ForschungszentrumJülich, Jülich, Germany

  11. Centre National de la Recherche Scientifique · Forschungszentrum Jülich · Czech Academy of Sciences · Commissariat à l'Énergie Atomique et aux Énergies Alternatives · FZU - Institute of Physics of the Czech Academy of Sciences · Institut de Biologie Structurale · Université Grenoble Alpes

    Affiliation as printed

    ELI Beamlines, Institute of Physics, Czech Academy of Sciences, Prague, Czech Republic

    Institut de Biologie Structurale (IBS), Université Grenoble Alpes-CEA-CNRS, Grenoble, France

    Institute of Biological Information Processing (IBI-7: Structural Biochemistry), ForschungszentrumJülich, Jülich, Germany

  12. Medizinische Hochschule Hannover

    Affiliation as printed

    Institute for Biophysical Chemistry, Hannover Medical School, Hannover, Germany

  13. Moscow Institute of Physics and Technology · Joint Institute for Nuclear Research

    Affiliation as printed

    Joint Institute for Nuclear Research, Dubna, Russia

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

  14. Moscow Institute of Physics and Technology

    Affiliation as printed

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

  15. Moscow Institute of Physics and Technology · Forschungszentrum Jülich

    Affiliation as printed

    Institute of Biological Information Processing (IBI-7: Structural Biochemistry), ForschungszentrumJülich, Jülich, Germany

    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich, Jülich, Germany

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

  16. Moscow Institute of Physics and Technology

    Affiliation as printed

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

  17. Moscow Institute of Physics and Technology

    Affiliation as printed

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

  18. National Institutes of Health · National Center for Biotechnology Information

    Affiliation as printed

    National Center for Biotechnology Information, National Library of Medicine, National Institutesof Health, Bethesda, MD, United States

  19. Max Planck Institute of Biophysics

    Affiliation as printed

    Max Planck Institute of Biophysics, Frankfurt am Main, Germany

  20. National Institutes of Health · National Center for Biotechnology Information

    Affiliation as printed

    National Center for Biotechnology Information, National Library of Medicine, National Institutesof Health, Bethesda, MD, United States

  21. Centre National de la Recherche Scientifique · Moscow Institute of Physics and Technology · Forschungszentrum Jülich · Commissariat à l'Énergie Atomique et aux Énergies Alternatives · Institut de Biologie Structurale · RWTH Aachen University · Université Grenoble Alpes

    Affiliation as printed

    Institut de Biologie Structurale (IBS), Université Grenoble Alpes-CEA-CNRS, Grenoble, France. valentin.gordeliy@ibs.fr

    Institute of Biological Information Processing (IBI-7: Structural Biochemistry), ForschungszentrumJülich, Jülich, Germany. valentin.gordeliy@ibs.fr

    Institute of Crystallography, University of Aachen (RWTH), Aachen, Germany. valentin.gordeliy@ibs.fr

    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich, Jülich, Germany. valentin.gordeliy@ibs.fr

    Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology, Dolgoprudny, Russia. valentin.gordeliy@ibs.fr

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

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References 86