TY - JOUR
T1 - Four principles to establish a universal virus taxonomy
AU - Simmonds, Peter
AU - Adriaenssens, Evelien M.
AU - Murilo Zerbini, F.
AU - Abrescia, Nicola G.A.
AU - Aiewsakun, Pakorn
AU - Alfenas-Zerbini, Poliane
AU - Bao, Yiming
AU - Barylski, Jakub
AU - Drosten, Christian
AU - Duffy, Siobain
AU - Paul Duprex, W.
AU - Dutilh, Bas E.
AU - Elena, Santiago F.
AU - García, Maria Laura
AU - Junglen, Sandra
AU - Katzourakis, Aris
AU - Koonin, Eugene V.
AU - Krupovic, Mart
AU - Kuhn, Jens H.
AU - Lambert, Amy J.
AU - Lefkowitz, Elliot J.
AU - Łobocka, Małgorzata
AU - Lood, Cédric
AU - Mahony, Jennifer
AU - Meier-Kolthoff, Jan P.
AU - Mushegian, Arcady R.
AU - Oksanen, Hanna M.
AU - Poranen, Minna M.
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
AU - Turner, Dann
AU - Van Doorslaer, Koenraad
AU - Vandamme, Anne Mieke
AU - Varsani, Arvind
AU - Vasilakis, Nikos
N1 - Funding Information:
Funding:TheworkshopandD.B.S.werefundedby aWellcomeBiomedicalResourcegranttoP.S.and S.S.(WT108418AIA).M.M.P.acknowledges fundingfromtheAcademyofFinland(grant 331627)andtheSigridJuse ´ liusFoundation.E.V.K. issupportedbytheIntramuralResearchProgram oftheUSNationalInstitutesofHealth(NIH) NationalLibraryofMedicine.Thisworkwas supportedinpartthroughLaulimaGovernment Solutions,LLCprimecontractwiththeUSNational InstituteofAllergyandInfectiousDiseases(NIAID) underContractNo.HHSN272201800013C.J.H.K. performedthisworkasanemployeeofTunnell GovernmentServices(TGS),asubcontractorof LaulimaGovernmentSolutions,LLCunder ContractNo.HHSN272201800013C.N.G.A.A.and S.F.E.aresupportedbytheAgenciaEstatalde Investigacio ´n (Spain) projects RTI2018-095700-BI00andPID2019-103998GB-I00,respectively.A.R.
Funding Information:
M.isaProgramDirectorattheUSNational ScienceFoundation(NSF),butthestatementsand opinionsexpressedhereinaremadeinthe personalcapacityanddonotconstitutethe endorsementbyNSForthegovernmentofthe USA.E.M.A.issupportedbytheBiotechnologyand BiologicalSciencesResearchCouncil(BBSRC); undertheBBSRCInstituteStrategicProgramGut MicrobesandHealthBB/R012490/1andits constituentprojectsBBS/E/F/000PR10353and BBS/E/F/000PR10356.D.L.R.acknowledges supportoftheUnitedKingdomMedicalResearch Council(MC_UU_1201412).S.S.acknowledges supportfromtheMississippiAgriculturaland ForestryExperimentStation(MAFES),USDA-ARS project58-6066-9-033,andtheNationalInstitute ofFoodandAgriculture,USDepartmentof Agriculture,HatchProject,underAccession Number1021494.J.M.issupportedbyScience FoundationIrelandunderGrantNumbers20/FFP-P/8664and15/SIRG/3430.N.V.acknowledges supportinpartbygrantsU01AI151807andR24 AI120942fromtheUSNIH.H.M.O.wassupported byUniversityofHelsinkifundingforFINStructand Instruct-ERICresearchinfrastructure.T.S. acknowledgessupportfromtheAustrianScience Fund(GrantNumberP28183).Thework conductedbytheUSDepartmentofEnergy(DOE) JointGenomeInstitute(S.R.),aDOEOfficeof ScienceUserFacility,issupportedbytheOfficeof ScienceoftheU.S.DepartmentofEnergyoperated underContractNo.DE-AC02-05CH11231.S.D. acknowledgessupportfromtheUSNational ScienceFoundation(DEB1453241,OIA1545553). B.E.D.wassupportedbytheEuropeanResearch Council(ERC)Consolidatorgrant865694-DiversiPHIandtheDeutsche Forschungsgemeinschaft(DFG,GermanResearch Foundation)underGermany’sExcellenceStrategy –EXC2051–Project-ID390713860,andthe AlexandervonHumboldtFoundationinthecontext ofanAlexandervonHumboldt-Professorship foundedbyGermanFederalMinistryofEducation andResearch.A.K.wassupportedbytheERC Consolidatorgrant101001623-PALVIREVOL. J.M.KwassupportedbyDeutsche Forschungsgemeinschaftwithin “SonderforschungsbereichTRR51”.E.J.L.was supportedbytheNIHNIAIDunderAwardNumber U24AI162625.C.L.wassupportedbya PostdoctoralMandate(PDMt2/21/038)fromthe KULeuvenResearchCouncilandafellowship (12D8623N)fromtheResearchFoundation– Flanders(FWO).M.B.S.wassupportedbytheUS NationalScienceFoundationawardsOCE#1829831 andABI#1759874.Y.B.wassupportedbythe ProfessionalAssociationoftheAllianceof
Publisher Copyright:
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PY - 2023/2
Y1 - 2023/2
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.
AB - 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.
KW - universal virus taxonomy
KW - principles
UR - http://www.scopus.com/inward/record.url?scp=85147927122&partnerID=8YFLogxK
U2 - 10.1371/journal.pbio.3001922
DO - 10.1371/journal.pbio.3001922
M3 - Article
C2 - 36780432
AN - SCOPUS:85147927122
SN - 1544-9173
VL - 21
JO - PLoS biology
JF - PLoS biology
IS - 2
M1 - e3001922
ER -