Four principles to establish a universal virus taxonomy

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 virolog...

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Vydané v:PLoS biology Ročník 21; číslo 2; s. e3001922
Hlavní autori: Simmonds, Peter, Adriaenssens, Evelien M., Zerbini, F. Murilo, Abrescia, Nicola G. A., Aiewsakun, Pakorn, Alfenas-Zerbini, Poliane, Bao, Yiming, Barylski, Jakub, Drosten, Christian, Duffy, Siobain, Duprex, W. Paul, Dutilh, Bas E., Elena, Santiago F., García, Maria Laura, Junglen, Sandra, Katzourakis, Aris, Koonin, Eugene V., Krupovic, Mart, Kuhn, Jens H., Lambert, Amy J., Lefkowitz, Elliot J., Łobocka, Małgorzata, Lood, Cédric, Mahony, Jennifer, Meier-Kolthoff, Jan P., Mushegian, Arcady R., Oksanen, Hanna M., Poranen, Minna M., Reyes-Muñoz, Alejandro, Robertson, David L., Roux, Simon, Rubino, Luisa, Sabanadzovic, Sead, Siddell, Stuart, Skern, Tim, Smith, Donald B., Sullivan, Matthew B., Suzuki, Nobuhiro, Turner, Dann, Van Doorslaer, Koenraad, Vandamme, Anne-Mieke, Varsani, Arvind, Vasilakis, Nikos
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States Public Library of Science 13.02.2023
Public Library of Science (PLoS)
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ISSN:1545-7885, 1544-9173, 1545-7885
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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.
AbstractList 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.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.
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.
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. Transforming an existing phenotypic classification of viruses into one based on evolutionary relationships that can accommodate the vast number of viruses characterized in metagenomics and environmental studies is an ongoing challenge. This Consensus View explains how such a taxonomy can be expanded to encapsulate viral diversity and to recognize independent biological origins of different virus groups.
Audience Academic
Author Aiewsakun, Pakorn
Elena, Santiago F.
Zerbini, F. Murilo
Skern, Tim
Adriaenssens, Evelien M.
Reyes-Muñoz, Alejandro
Siddell, Stuart
Meier-Kolthoff, Jan P.
Łobocka, Małgorzata
Dutilh, Bas E.
Lefkowitz, Elliot J.
Simmonds, Peter
Lood, Cédric
Krupovic, Mart
Poranen, Minna M.
Turner, Dann
Robertson, David L.
Duprex, W. Paul
Rubino, Luisa
Sullivan, Matthew B.
Bao, Yiming
Koonin, Eugene V.
Abrescia, Nicola G. A.
Drosten, Christian
Barylski, Jakub
Mushegian, Arcady R.
Smith, Donald B.
Alfenas-Zerbini, Poliane
Oksanen, Hanna M.
Junglen, Sandra
Suzuki, Nobuhiro
Lambert, Amy J.
Van Doorslaer, Koenraad
Varsani, Arvind
Duffy, Siobain
Vandamme, Anne-Mieke
Vasilakis, Nikos
García, Maria Laura
Mahony, Jennifer
Katzourakis, Aris
Kuhn, Jens H.
Sabanadzovic, Sead
Roux, Simon
AuthorAffiliation 22 Institut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology Unit, Paris, France
38 Medical University of Vienna, Max Perutz Labs, Vienna Biocenter, Vienna, Austria
7 Departamento de Microbiologia/BIOAGRO, Universidade Federal de Viçosa, Viçosa, Brazil
20 Department of Biology, University of Oxford, Oxford, United Kingdom
33 MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom
14 The Center for Vaccine Research, University of Pittsburgh School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America
41 School of Applied Sciences, College of Health, Science and Society, University of the West of England, Bristol, United Kingdom
19 Instituto de Biotecnología y Biología Molecular, CCT-La Plata, CONICET, UNLP, La Plata, Argentina
26 Institute of Biochemistry and Biophysics of the Polish Academy of Sciences, Warsaw, Poland
1 Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
9 University of Chinese Acad
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– name: 18 Santa Fe Institute, Santa Fe, New Mexico, United States of America
– name: 38 Medical University of Vienna, Max Perutz Labs, Vienna Biocenter, Vienna, Austria
– name: 24 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
– name: 23 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
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– name: 1 Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
– name: 4 Structure and Cell Biology of Viruses Lab, Center for Cooperative Research in Biosciences—BRTA, Derio, Spain
– name: 3 Departamento de Fitopatologia/BIOAGRO, Universidade Federal de Viçosa, Viçosa, Brazil
– name: 35 Istituto per la Protezione Sostenibile delle Piante, CNR, UOS Bari, Bari, Italy
– name: 19 Instituto de Biotecnología y Biología Molecular, CCT-La Plata, CONICET, UNLP, La Plata, Argentina
– name: 25 Department of Microbiology, University of Alabama at Birmingham, Birmingham, Alabama, United States of America
– name: 45 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
– name: 13 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
– name: 26 Institute of Biochemistry and Biophysics of the Polish Academy of Sciences, Warsaw, Poland
– name: 40 Institute of Plant Science and Resources, Okayama University, Kurashiki, Okayama, Japan
– name: 2 Quadram Institute Bioscience, Norwich Research Park, Norwich, United Kingdom
– name: 11 Institute of Virology, Charité-Universitätsmedizin Berlin, corporate member of Free University Berlin, Humboldt University, Berlin, Germany
– name: 30 Division of Molecular and Cellular Biosciences, National Science Foundation, Alexandria, Virginia, United States of America
– name: 17 Instituto de Biología Integrativa de Sistemas (I2SysBio), CSIC-Universitat de València, Valencia, Spain
– name: 46 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
– name: 33 MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom
– name: 44 Center for Global Health and Tropical Medicine, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Lisbon, Portugal
– name: 27 Department of Biosystems, KU Leuven, Leuven, Belgium
– name: 20 Department of Biology, University of Oxford, Oxford, United Kingdom
– name: 41 School of Applied Sciences, College of Health, Science and Society, University of the West of England, Bristol, United Kingdom
– name: 21 National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, United States of America
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– name: 9 University of Chinese Academy of Sciences, Beijing, China
– name: 10 Department of Molecular Virology, Adam Mickiewicz University, Poznan, Poland
– name: 34 Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, California, United States of America
– name: 6 Department of Microbiology, Faculty of Science, Mahidol University, Bangkok, Thailand
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/36780432$$D View this record in MEDLINE/PubMed
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SubjectTerms Analysis
Bacteriophages
BASIC BIOLOGICAL SCIENCES
Biology
Biology and Life Sciences
Classification
Communication
Computer and Information Sciences
Consensus View
Debates
Epidemiology
Evolution
evolutionary genetics
evolutionary systematics
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Humans
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Immunodeficiency
Life Sciences
Metagenomics
Nomenclature
Pathogenicity
Pathogens
Phages
Phenetics
phylogenetics
Phylogeny
Principles
Quality control
RNA viruses
Taxonomy
viral evolution
viral genomics
viral taxonomy
Viruses
Viruses - genetics
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Title Four principles to establish a universal virus taxonomy
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