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

doi:10.1371/journal.pbio.3001922

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 LambertElliot 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

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

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.

Original language	English
Article number	e3001922
Number of pages	23
Journal	PLoS Biology
Volume	21
Issue number	2
DOIs	https://doi.org/10.1371/journal.pbio.3001922
Publication status	Published - Feb 2023

Bibliographical note

Publisher Copyright:
Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Funding

The workshop and D.B.S. were funded by a Wellcome Biomedical Resource grant to P.S. and S.S. (WT108418AIA). M.M.P. acknowledges funding from the Academy of Finland (grant 331627) and the Sigrid Juselius Foundation. E.V.K. is supported by the Intramural Research Program of the US National Institutes of Health (NIH) National Library of Medicine. This work was supported in part through Laulima Government Solutions, LLC prime contract with the US National Institute of Allergy and Infectious Diseases (NIAID) under Contract No. HHSN272201800013C. J.H.K. performed this work as an employee of Tunnell Government Services (TGS), a subcontractor of Laulima Government Solutions, LLC under Contract No. HHSN272201800013C. N.G.A.A. and S.F.E. are supported by the Agencia Estatal de Investigacian (Spain) projects RTI2018-095700-B-I00 and PID2019-103998GB-I00, respectively. A.R. M. is a Program Director at the US National Science Foundation (NSF), but the statements and opinions expressed herein are made in the personal capacity and do not constitute the endorsement by NSF or the government of the USA. E.M.A. is supported by the Biotechnology and Biological Sciences Research Council (BBSRC); under the BBSRC Institute Strategic Program Gut Microbes and Health BB/R012490/1 and its constituent projects BBS/E/F/000PR10353 and BBS/E/F/000PR10356. D.L.R. acknowledges support of the United Kingdom Medical Research Council (MC_UU_1201412). S.S. acknowledges support from the Mississippi Agricultural and Forestry Experiment Station (MAFES), USDA-ARS project 58-6066-9-033, and the National Institute of Food and Agriculture, US Department of Agriculture, Hatch Project, under Accession Number 1021494. J.M. is supported by Science Foundation Ireland under Grant Numbers 20/FFP-P/8664 and 15/SIRG/3430. N.V. acknowledges support in part by grants U01 AI151807 and R24 AI120942 from the US NIH. H.M.O. was supported by University of Helsinki funding for FINStruct and Instruct-ERIC research infrastructure. T.S. acknowledges support from the Austrian Science Fund (Grant Number P 28183). The work conducted by the US Department of Energy (DOE) Joint Genome Institute (S.R.), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231. S.D. acknowledges support from the US National Science Foundation (DEB 1453241, OIA 1545553). B.E.D. was supported by the European Council (ERC) Consolidator grant 865694-DiversiPHI and the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany's Excellence Strategy - EXC 2051 - Project-ID 390713860, and the Alexander von Humboldt Foundation in the context of an Alexander von Humboldt-Professorship founded by German Federal Ministry of Education and Research. A.K. was supported by the ERC Consolidator grant 101001623-PALVIREVOL. J.M.K was supported by Deutsche Forschungsgemeinschaft within "Sonderforschungsbereich TRR 51". E.J.L. was supported by the NIH NIAID under Award Number U24AI162625. C.L. was supported by a Postdoctoral Mandate (PDMt2/21/038) from the KU Leuven Research Council and a fellowship (12D8623N) from the Research Foundation - Flanders (FWO). M.B.S. was supported by the US National Science Foundation awards OCE#1829831 and ABI#1759874. Y.B. was supported by the Professional Association of the Alliance of International Science Organizations (ANSO-PA-2020-07) and the Open Biodiversity and Health Big Data Programme of IUBS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Funders	Funder number
Wellcome Biomedical Resource grant	WT108418AIA
Academy of Finland	331627
Sigrid Juselius Foundation
Intramural Research Program of the US National Institutes of Health (NIH) National Library of Medicine
US National Institute of Allergy and Infectious Diseases (NIAID)	HHSN272201800013C
Biotechnology and Biological Sciences Research Council (BBSRC)	BBS/E/F/000PR10356, MC_UU_1201412, 58-6066-9-033
United Kingdom Medical Research Council	1021494
Laulima Government Solutions, LLC
Mississippi Agricultural and Forestry Experiment Station (MAFES)
Agencia Estatal de Investigacian (Spain)	20/FFP-P/8664
USDA-ARS project
US National Science Foundation	15/SIRG/3430
National Institute of Food and Agriculture, US Department of Agriculture, Hatch Project
Science Foundation Ireland	P 28183, DE-AC02-05CH11231
US NIH	RTI2018-095700-B-I00, PID2019-103998GB-I00
University of Helsinki
Austrian Science Fund	101001623-PALVIREVOL
Office of Science of the U.S. Department of Energy	U24AI162625
US National Science Foundation	1829831, 1759874
European Research Council (ERC) Consolidator grant	R24 AI120942
Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany's Excellence Strategy	DEB 1453241
Alexander von Humboldt Foundation
ERC Consolidator grant	OIA 1545553
Deutsche Forschungsgemeinschaft
NIH NIAID	Sonderforschungsbereich TRR 51
KU Leuven Research Council
Research Foundation - Flanders (FWO)
Professional Association of the Alliance of International Science Organizations	HHSN272201800013C
Open Biodiversity and Health Big Data Programme of IUBS
Not added	BB/R012490/1
Not added	BBS/E/F/000PR10353
Not added	865694-DiversiPHI
Not added	390713860
Not added	ANSO-PA-2020-07
Not added	U01 AI151807
Not added	EXC 2051
Not added	PDMt2/21/038
Not added	12D8623N

Keywords

Humans
Bacteriophages
Metagenomics
Phylogeny
Viruses/genetics

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10.1371/journal.pbio.3001922Licence: CC0

journal.pbio.3001922Final published version, 1.78 MBLicence: CC0

Cite this

Simmonds, P., Adriaenssens, E. M., Zerbini, F. M., Abrescia, N. G. A., Aiewsakun, P., Alfenas-Zerbini, P., Bao, Y., Barylski, J., Drosten, C., Duffy, S., Duprex, W. P., Dutilh, B. E., Elena, S. F., García, M. L., Junglen, S., Katzourakis, A., Koonin, E. V., Krupovic, M., Kuhn, J. H., ... Vasilakis, N. (2023). Four principles to establish a universal virus taxonomy. PLoS Biology, 21(2), Article e3001922. https://doi.org/10.1371/journal.pbio.3001922

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Simmonds, P, Adriaenssens, EM, Zerbini, FM, Abrescia, NGA, Aiewsakun, P, Alfenas-Zerbini, P, Bao, Y, Barylski, J, Drosten, C, Duffy, S, Duprex, WP, Dutilh, BE, Elena, SF, García, ML, Junglen, S, Katzourakis, A, Koonin, EV, Krupovic, M, Kuhn, JH, Lambert, AJ, Lefkowitz, EJ, Łobocka, M, Lood, C, Mahony, J, Meier-Kolthoff, JP, Mushegian, AR, Oksanen, HM, Poranen, MM, Reyes-Muñoz, A, Robertson, DL, Roux, S, Rubino, L, Sabanadzovic, S, Siddell, S, Skern, T, Smith, DB, Sullivan, MB, Suzuki, N, Turner, D, Van Doorslaer, K, Vandamme, A-M, Varsani, A & Vasilakis, N 2023, 'Four principles to establish a universal virus taxonomy', PLoS Biology, vol. 21, no. 2, e3001922. https://doi.org/10.1371/journal.pbio.3001922

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AU - Reyes-Muñoz, Alejandro

AU - Robertson, David L

AU - Roux, Simon

AU - Rubino, Luisa

AU - Sabanadzovic, Sead

AU - Siddell, Stuart

AU - Skern, Tim

AU - Smith, Donald B

AU - Sullivan, Matthew B

AU - Suzuki, Nobuhiro

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AU - Van Doorslaer, Koenraad

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AU - Varsani, Arvind

AU - Vasilakis, Nikos

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N2 - 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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Four principles to establish a universal virus taxonomy

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Keywords

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