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02, 2023;21 (2): e3001922.

Four principles to establish a universal virus taxonomy.

Peter Simmonds, Evelien M Adriaenssens, F Murilo Zerbini, Nicola G A Abrescia, Pakorn Aiewsakun, Poliane Alfenas-Zerbini, Yiming Bao, Jakub Barylski, Christian Drosten, Siobain Duffy, W Paul Duprex, Bas E Dutilh, Santiago F Elena, Maria Laura García, Sandra Junglen, Aris Katzourakis, Eugene V Koonin, Mart Krupovic, Jens H Kuhn, Amy J Lambert, Elliot J Lefkowitz, Małgorzata Łobocka, Cédric Lood, Jennifer Mahony, Jan P Meier-Kolthoff, Arcady R Mushegian, Hanna M Oksanen, Minna M Poranen, Alejandro Reyes-Muñoz, David L Robertson, Simon Roux, Luisa Rubino, Sead Sabanadzovic, Stuart Siddell, Tim Skern, Donald B Smith, Matthew B Sullivan, Nobuhiro Suzuki, Dann Turner, Koenraad Van Doorslaer, Anne-Mieke Vandamme, Arvind Varsani, Nikos Vasilakis
Author Information
  1. Peter Simmonds: Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom. ORCID
  2. Evelien M Adriaenssens: Quadram Institute Bioscience, Norwich Research Park, Norwich, United Kingdom.
  3. F Murilo Zerbini: Departamento de Fitopatologia/BIOAGRO, Universidade Federal de Viçosa, Viçosa, Brazil.
  4. Nicola G A Abrescia: Structure and Cell Biology of Viruses Lab, Center for Cooperative Research in Biosciences-BRTA, Derio, Spain.
  5. Pakorn Aiewsakun: Department of Microbiology, Faculty of Science, Mahidol University, Bangkok, Thailand.
  6. Poliane Alfenas-Zerbini: Departamento de Microbiologia/BIOAGRO, Universidade Federal de Viçosa, Viçosa, Brazil.
  7. Yiming Bao: National Genomics Data Center, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing, China.
  8. Jakub Barylski: Department of Molecular Virology, Adam Mickiewicz University, Poznan, Poland.
  9. Christian Drosten: Institute of Virology, Charité-Universitätsmedizin Berlin, corporate member of Free University Berlin, Humboldt University, Berlin, Germany.
  10. Siobain Duffy: Department of Ecology, Evolution and Natural Resources, School of Environmental and Biological Sciences, Rutgers The State University of New Jersey, New Brunswick, New Jersey, United States of America.
  11. W Paul Duprex: The Center for Vaccine Research, University of Pittsburgh School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
  12. Bas E Dutilh: Institute of Biodiversity, Faculty of Biological Sciences, Cluster of Excellence Balance of the Microverse, Friedrich-Schiller-University, Jena, Germany.
  13. Santiago F Elena: Instituto de Biología Integrativa de Sistemas (I2SysBio), CSIC-Universitat de València, Valencia, Spain.
  14. Maria Laura García: Instituto de Biotecnología y Biología Molecular, CCT-La Plata, CONICET, UNLP, La Plata, Argentina.
  15. Sandra Junglen: Institute of Virology, Charité-Universitätsmedizin Berlin, corporate member of Free University Berlin, Humboldt University, Berlin, Germany.
  16. Aris Katzourakis: Department of Biology, University of Oxford, Oxford, United Kingdom.
  17. Eugene V Koonin: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, United States of America.
  18. Mart Krupovic: Institut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology Unit, Paris, France.
  19. Jens H Kuhn: Integrated Research Facility at Fort Detrick (IRF-Frederick), National Institute of Allergy and Infectious Diseases, National Institutes of Health, Fort Detrick, Frederick, Maryland, United States of America.
  20. Amy J Lambert: Division of Vector-Borne Diseases, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado, United States of America.
  21. Elliot J Lefkowitz: Department of Microbiology, University of Alabama at Birmingham, Birmingham, Alabama, United States of America.
  22. Małgorzata Łobocka: Institute of Biochemistry and Biophysics of the Polish Academy of Sciences, Warsaw, Poland.
  23. Cédric Lood: Department of Biosystems, KU Leuven, Leuven, Belgium.
  24. Jennifer Mahony: School of Microbiology and APC Microbiome Ireland, University College Cork, Cork, Ireland.
  25. Jan P Meier-Kolthoff: Department of Bioinformatics and Databases, Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures GmbH, Braunschweig, Germany.
  26. Arcady R Mushegian: Division of Molecular and Cellular Biosciences, National Science Foundation, Alexandria, Virginia, United States of America.
  27. Hanna M Oksanen: Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland.
  28. Minna M Poranen: Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland.
  29. Alejandro Reyes-Muñoz: Max Planck Tandem Group in Computational Biology, Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá, Colombia.
  30. David L Robertson: MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom.
  31. Simon Roux: Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, California, United States of America.
  32. Luisa Rubino: Istituto per la Protezione Sostenibile delle Piante, CNR, UOS Bari, Bari, Italy.
  33. Sead Sabanadzovic: Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, Mississippi, United States of America.
  34. Stuart Siddell: School of Cellular and Molecular Medicine, Faculty of Life Sciences, University of Bristol, Bristol, United Kingdom.
  35. Tim Skern: Medical University of Vienna, Max Perutz Labs, Vienna Biocenter, Vienna, Austria.
  36. Donald B Smith: Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom.
  37. Matthew B Sullivan: Departments of Microbiology and Civil, Environmental, and Geodetic Engineering, Ohio State University, Columbus, Ohio, United States of America.
  38. Nobuhiro Suzuki: Institute of Plant Science and Resources, Okayama University, Kurashiki, Okayama, Japan.
  39. Dann Turner: School of Applied Sciences, College of Health, Science and Society, University of the West of England, Bristol, United Kingdom.
  40. Koenraad Van Doorslaer: School of Animal and Comparative Biomedical Sciences, Department of Immunobiology, BIO5 Institute, and University of Arizona Cancer Center, Tucson, Arizona, United States of America.
  41. Anne-Mieke Vandamme: KU Leuven, Department of Microbiology, Immunology and Transplantation, Rega Institute for Medical Research, Leuven, Belgium.
  42. Arvind Varsani: The Biodesign Center for Fundamental and Applied Microbiomics, School of Life Sciences, Center for Evolution and Medicine, Arizona State University, Tempe, Arizona, United States of America.
  43. Nikos Vasilakis: Department of Pathology, Center of Vector-Borne and Zoonotic Diseases, Institute for Human Infection and Immunity and World Reference Center for Emerging Viruses and Arboviruses, The University of Texas Medical Branch, Galveston, Texas, United States of America.
PMID: 36780432 DOI: 10.1371/journal.pbio.3001922

Abstract

A universal taxonomy of viruses is essential for a comprehensive view of the virus world and for communicating the complicated evolutionary relationships among viruses. However, there are major differences in the conceptualisation and approaches to virus classification and nomenclature among virologists, clinicians, agronomists, and other interested parties. Here, we provide recommendations to guide the construction of a coherent and comprehensive virus taxonomy, based on expert scientific consensus. Firstly, assignments of viruses should be congruent with the best attainable reconstruction of their evolutionary histories, i.e., taxa should be monophyletic. This fundamental principle for classification of viruses is currently included in the International Committee on Taxonomy of Viruses (ICTV) code only for the rank of species. Secondly, phenotypic and ecological properties of viruses may inform, but not override, evolutionary relatedness in the placement of ranks. Thirdly, alternative classifications that consider phenotypic attributes, such as being vector-borne (e.g., "arboviruses"), infecting a certain type of host (e.g., "mycoviruses," "bacteriophages") or displaying specific pathogenicity (e.g., "human immunodeficiency viruses"), may serve important clinical and regulatory purposes but often create polyphyletic categories that do not reflect evolutionary relationships. Nevertheless, such classifications ought to be maintained if they serve the needs of specific communities or play a practical clinical or regulatory role. However, they should not be considered or called taxonomies. Finally, while an evolution-based framework enables viruses discovered by metagenomics to be incorporated into the ICTV taxonomy, there are essential requirements for quality control of the sequence data used for these assignments. Combined, these four principles will enable future development and expansion of virus taxonomy as the true evolutionary diversity of viruses becomes apparent.

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Grants

  1. U24 AI162625/NIAID NIH HHS
  2. MC_UU_12014/12/Medical Research Council
  3. U01 AI151807/NIAID NIH HHS
  4. R24 AI120942/NIAID NIH HHS
  5. BBS/E/F/000PR10353/Biotechnology and Biological Sciences Research Council
  6. BBS/E/F/000PR10356/Biotechnology and Biological Sciences Research Council
  7. BB/R012490/1/Biotechnology and Biological Sciences Research Council
  8. /Wellcome Trust
  9. HHSN272201800013C/NIAID NIH HHS

MeSH Term

Humans
Bacteriophages
Metagenomics
Phylogeny
Viruses
Journal Article Research Support, N.I.H., Intramural Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

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