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Unique structure and function of viral rhodopsins

  • Dmitry Bratanov
  • , Kirill Kovalev
  • , Jan-Philipp Machtens
  • , Roman Astashkin
  • , Igor Chizhov
  • , Dmytro Soloviov
  • , Dmytro Volkov
  • , Vitaly Polovinkin
  • , Dmitrii Zabelskii
  • , Thomas Mager
  • , Ivan Gushchin
  • , Tatyana Rokitskaya
  • , Yuri Antonenko
  • , Alexey Alekseev
  • , Vitaly Shevchenko
  • , Natalya Yutin
  • , Riccardo Rosselli
  • , Christian Baeken
  • , Valentin Borshchevskiy
  • , Gleb Bourenkov
  • Alexander Popov, Taras Balandin, Georg Büldt, Dietmar J. Manstein, Francisco Rodriguez-Valera, Christoph Fahlke, Ernst Bamberg, Eugene Koonin, Valentin Gordeliy

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Recently, two groups of rhodopsin genes were identified in large double-stranded DNA viruses. The structure and function of viral rhodopsins are unknown. We present functional characterization and high-resolution structure of an Organic Lake Phycodnavirus rhodopsin II (OLPVRII) of group 2. It forms a pentamer, with a symmetrical, bottle-like central channel with the narrow vestibule in the cytoplasmic part covered by a ring of 5 arginines, whereas 5 phenylalanines form a hydrophobic barrier in its exit. The proton donor E42 is placed in the helix B. The structure is unique among the known rhodopsins. Structural and functional data and molecular dynamics suggest that OLPVRII might be a light-gated pentameric ion channel analogous to pentameric ligand-gated ion channels, however, future patch clamp experiments should prove this directly. The data shed light on a fundamentally distinct branch of rhodopsins and may contribute to the understanding of virus-host interactions in ecologically important marine protists.
Original languageEnglish
Article number4939
JournalNature Communications
Volume10
Issue number1
DOIs
Publication statusPublished - 1 Dec 2019
Externally publishedYes

Funding

We are grateful to Dr. Igor Melnikov for obtaining the original molecular replacement solution. We acknowledge the Structural Biology Group of the European Synchrotron Radiation Facility (ESRF) and The European Molecular Biology Laboratory (EMBL) unit in Hamburg at Deutsche Elektronen-Synchrotron (DESY) for granting access to the synchrotron beamlines. This work was supported by the common program of Agence Nationale de la Recherche (ANR), France and Deutsche Forschungsgemeinschaft (DFG), Germany (ANR-15-CE11-0029-02/FA 301/11-1), by the DFG Research Unit FOR 2518 (DynIon, project P4 to JPM, MA 7525/1-1), and by funding from Frankfurt: Cluster of Excellence Frankfurt Macromolecular Complexes by the Max Planck Society (to E.B.) and by the Commissariat à l’Energie Atomique et aux Energies Alternatives (Institut de Biologie Structurale)–Helmholtz-Gemeinschaft Deutscher Forschungszentren (For-schungszentrum Jülich) Special Terms and Conditions 5.1 specific agreement. This work used the platforms of the Grenoble Instruct-ERIC center (ISBG; UMS 3518 CNRS-CEA-UJF-EMBL) within the Grenoble Partnership for Structural Biology (PSB). Platform access was supported by FRISBI (ANR-10-INBS-05-02) and GRAL, a project of the University Grenoble Alpes graduate school (Ecoles Universitaires de Recherche) CBH-EUR-GS (ANR-17-EURE-0003). Spectroscopic characterization, time-resolved absorption spectroscopy, and crosslinking experiments were supported by RSF-DFG grant (Helmholtz—RSF Joint Research Groups grant (RSF No. 19-44-06302)). D.B. was supported by grant ANR-14-CE09-0028. F.R.-V. was supported by grant VIREVO CGL2016‐76273‐P (AEI/FEDER, EU) (co-founded with FEDER funds). D.J.M. was funded by the Deutsche Forschungsgemeinschaft under Germany’s Excellence Strategy— EXC 2155 “RESIST”—Project ID 39087428. N.Y. and E.K. are funded through the Intramural Research Program of the National Institutes of Health of the USA. V.B. is thankful to the Ministry of Science and Higher Education of the Russian Federation (project № 6.9909.2017/6.7) for personal support. K.K., A.A., I.G., V.B., D.Z. were supported by grant 17-00-00164komfi (Russian Foundation for Basic Research). D.Z. and R.A. were supported by grant 6.3157.2017 (the Ministry of Science and High Education of the Russian Federation). The authors gratefully acknowledge the computing time granted by the JARA-HPC Vergabegremium and VSR commission on the supercomputer JURECA at Forschungszentrum Jülich.

FundersFunder number
RSF-DFG
Max-Planck-Gesellschaft
Helmholtz-Gemeinschaft
Commissariat à l'Énergie Atomique et aux Énergies Alternatives
National Institutes of Health
Agencia Estatal de Investigación
French Infrastructure for Integrated Structural Biology
For-schungszentrum Jülich
Helmholtz
Institut de Biologie Structurale
Ministry of Science and Higher Education of the Russian Federation
Deutsche ForschungsgemeinschaftFOR 2518, ANR-15-CE11-0029-02/FA 301/11-1, MA 7525/1-1
Agence Nationale de la RechercheANR-15-CE11-0029, ANR-14-CE09-0028, ANR-17-EURE-0003, ANR-10-INBS-05-02, ANR-15-CE11-0029-02
Russian Science FoundationRSF №19-44-06302, 19-44-06302
European Regional Development Fund39087428, EXC 2155
Ministry of Education and Science of the Russian Federation17-00-00164komfi, 6.9909.2017/6.7
Russian Foundation for Basic Research6.3157.2017

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