Virus nomenclature below the species level: a standardized nomenclature for natural variants of viruses assigned to the family Filoviridae

Jens H Kuhn, Yiming Bao, Sina Bavari, Stephan Becker, Steven Bradfute, J Rodney Brister, Alexander A Bukreyev, Kartik Chandran, Robert A Davey, Olga Dolnik, John M Dye, Sven Enterlein, Lisa E Hensley, Anna N Honko, Peter B Jahrling, Karl M Johnson, Gary Kobinger, Eric M Leroy, Mark S Lever, Elke Mühlberger, Sergey V Netesov, Gene G Olinger, Gustavo Palacios, Jean L Patterson, Janusz T Paweska, Louise Pitt, Sheli R Radoshitzky, Erica Ollmann Saphire, Sophie J Smither, Robert Swanepoel, Jonathan S Towner, Guido van der Groen, Viktor E Volchkov, Victoria Wahl-Jensen, Travis K Warren, Manfred Weidmann, Stuart T Nichol, Jens H Kuhn, Yiming Bao, Sina Bavari, Stephan Becker, Steven Bradfute, J Rodney Brister, Alexander A Bukreyev, Kartik Chandran, Robert A Davey, Olga Dolnik, John M Dye, Sven Enterlein, Lisa E Hensley, Anna N Honko, Peter B Jahrling, Karl M Johnson, Gary Kobinger, Eric M Leroy, Mark S Lever, Elke Mühlberger, Sergey V Netesov, Gene G Olinger, Gustavo Palacios, Jean L Patterson, Janusz T Paweska, Louise Pitt, Sheli R Radoshitzky, Erica Ollmann Saphire, Sophie J Smither, Robert Swanepoel, Jonathan S Towner, Guido van der Groen, Viktor E Volchkov, Victoria Wahl-Jensen, Travis K Warren, Manfred Weidmann, Stuart T Nichol

Abstract

The task of international expert groups is to recommend the classification and naming of viruses. The International Committee on Taxonomy of Viruses Filoviridae Study Group and other experts have recently established an almost consistent classification and nomenclature for filoviruses. Here, further guidelines are suggested to include their natural genetic variants. First, this term is defined. Second, a template for full-length virus names (such as “Ebola virus H.sapiens-tc/COD/1995/Kikwit-9510621”) is proposed. These names contain information on the identity of the virus (e.g., Ebola virus), isolation host (e.g., members of the species Homo sapiens), sampling location (e.g., Democratic Republic of the Congo (COD)), sampling year, genetic variant (e.g., Kikwit), and isolate (e.g., 9510621). Suffixes are proposed for individual names that clarify whether a given genetic variant has been characterized based on passage zero material (-wt), has been passaged in tissue/cell culture (-tc), is known from consensus sequence fragments only (-frag), or does (most likely) not exist anymore (-hist). We suggest that these comprehensive names are to be used specifically in the methods section of publications. Suitable abbreviations, also proposed here, could then be used throughout the text, while the full names could be used again in phylograms, tables, or figures if the contained information aids the interpretation of presented data. The proposed system is very similar to the well-known influenzavirus nomenclature and the nomenclature recently proposed for rotaviruses. If applied consistently, it would considerably simplify retrieval of sequence data from electronic databases and be a first important step toward a viral genome annotation standard as sought by the National Center for Biotechnology Information (NCBI). Furthermore, adoption of this nomenclature would increase the general understanding of filovirus-related publications and presentations and improve figures such as phylograms, alignments, and diagrams. Most importantly, it would counter the increasing confusion in genetic variant naming due to the identification of ever more sequences through technological breakthroughs in high-throughput sequencing and environmental sampling.

References

    1. Adams MJ, Carstens EB. Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses 2012. Arch Virol. 2012;157:1411–1422. doi: 10.1007/s00705-012-1299-6.
    1. Barrette RW, Metwally SA, Rowland JM, Xu L, Zaki SR, Nichol ST, Rollin PE, Towner JS, Shieh W-J, Batten B, Sealy TK, Carrillo C, Moran KE, Bracht AJ, Mayr GA, Sirios-Cruz M, Catbagan DP, Lautner EA, Ksiazek TG, White WR, McIntosh MT. Discovery of swine (sic) as a host for the Reston ebolavirus (sic) Science. 2009;325:204–206. doi: 10.1126/science.1172705.
    1. Brister JR, Bao Y, Kuiken C, Lefkowitz EJ, le Mercier P, Leplae R, Madupu R, Scheuermann RH, Schobel S, Seto D, Shrivastava S, Sterk P, Zeng Q, Klimke W, Tatusova T. Towards viral genome annotation standards, report from the 2010 NCBI annotation workshop. Viruses. 2010;2:2258–2268. doi: 10.3390/v2102258.
    1. Calisher CH, Mahy BWJ. Taxonomy: get it right or leave it alone. Am J Trop Med Hyg. 2003;68:505–506.
    1. Calisher CH, van Regenmortel MHV. Should all other biologists follow the lead of virologists and stop italicizing the names of living organisms? Zootaxa. 2009;2113:63–68.
    1. Cavanagh D. A nomenclature for avian coronavirus isolates and the question of species status. Avian Pathol. 2001;30:109–115. doi: 10.1080/03079450120044506.
    1. Drebot MA, Henchal E, Hjelle B, LeDuc JW, Repik PM, Roehrig JT, Schmaljohn CS, Shope RE, Tesch RB, Weaver SC, Calisher CH. Improved clarity of meaning from the use of both formal species names and common (vernacular) virus names in virological literature. Arch Virol. 2002;147:2465–2471. doi: 10.1007/s00705-002-0938-8.
    1. Fauquet CM, Stanley J. Revising the way we conceive and name viruses below the species level: a review of geminivirus taxonomy calls for new standardized isolate descriptors. Arch Virol. 2005;150:2151–2179. doi: 10.1007/s00705-005-0583-0.
    1. Fauquet CM, Briddon RW, Brown JK, Moriones E, Stanley J, Zerbini M, Zhou X. Geminivirus strain demarcation and nomenclature. Arch Virol. 2008;153:783–821. doi: 10.1007/s00705-008-0037-6.
    1. Feldmann H, Geisbert TW, Jahrling PB, Klenk H-D, Netesov SV, Peters CJ, Sanchez A, Swanepoel R, Volchkov VE. Family filoviridae. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA, editors. Virus taxonomy—eighth report of the International Committee on Taxonomy of viruses. San Diego: Elsevier/Academic Press; 2005. pp. 645–653.
    1. Green KY, Ando T, Balayan MS, Berke T, Clarke IN, Estes MK, Matson DO, Nakata S, Neill JD, Studdert MJ, Thiel H-J. Taxonomy of the caliciviruses. J Infect Dis. 2000;181(suppl 2):S322–S330. doi: 10.1086/315591.
    1. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, editors. Virus taxonomy—ninth report of the International Committee on Taxonomy of viruses. London: Elsevier/Academic Press; 2011.
    1. Kuhn JH (2008) Filoviruses—a compendium of 40 years of epidemiological, clinical, and laboratory studies. Arch Virol Suppl, vol 20. Springer, Wien
    1. Kuhn JH, Becker S, Ebihara H, Geisbert TW, Johnson KM, Lipkin WI, Negredo A, Netesov SV, Nichol ST, Palacios G, Peters CJ, Tenorio A, Volchkov VE, Jahrling PB. Proposal for a revised taxonomy of the family Filoviridae: classification, names of taxa and viruses, and virus abbreviations. Arch Virol. 2010;155:2083–2103. doi: 10.1007/s00705-010-0814-x.
    1. Kuhn JH, Jahrling PB. Clarification and guidance on the proper usage of virus and virus species names. Arch Virol. 2010;155:445–453. doi: 10.1007/s00705-010-0600-9.
    1. Kuhn JH, Wahl-Jensen V. Being obsessive-compulsive about terminology and nomenclature is not a vice, but a virtue. Bionomina. 2010;1:11–14.
    1. Kuhn JH, Becker S, Ebihara H, Geisbert TW, Jahrling PB, Kawaoka Y, Netesov SV, Nichol ST, Peters CJ, Volchkov VE, Ksiazek TG. Family Filoviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, editors. Virus Taxonomy - Ninth Report of the International Committee on Taxonomy of Viruses. London: Elsevier/Academic Press; 2011. pp. 665–671.
    1. Kuhn JH, Dodd LE, Wahl-Jensen V, Radoshitzky SR, Bavari S, Jahrling PB. Evaluation of perceived threat differences posed by filovirus variants. Biosecur Bioterror. 2011;9:361–371. doi: 10.1089/bsp.2011.0051.
    1. Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, Yaba P, Délicat A, Paweska JT, Gonzalez J-P, Swanepoel R. Fruit bats as reservoirs of Ebola virus. Nature. 2005;438:575–576. doi: 10.1038/438575a.
    1. Maniloff J. Identification and classification of viruses that have not been propagated. Arch Virol. 1995;140:1515–1520. doi: 10.1007/BF01322679.
    1. Matthijnssens J, Ciarlet M, McDonald SM, Attoui H, Banyai K, Brister JR, Buesa J, Esona MD, Estes MK, Gentsch JR, Iturriza-Gomara M, Johne R, Kirkwood CD, Martella V, Mertens PP, Nakagomi O, Parreno V, Rahman M, Ruggeri FM, Saif LJ, Santos N, Steyer A, Taniguchi K, Patton JT, Desselberger U, Van Ranst M. Uniformity of rotavirus strain nomenclature proposed by the Rotavirus classification working group (RCWG) Arch Virol. 2011;156:1397–1413. doi: 10.1007/s00705-011-1006-z.
    1. Negredo A, Palacios G, Vazquez-Moron S, Gonzalez F, Dopazo H, Molero F, Juste J, Quetglas J, Savji N, de la Cruz Martinez M, Herrera JE, Pizarro M, Hutchison SK, Echevarria JE, Lipkin WI, Tenorio A. Discovery of an Ebola virus-like filovirus in Europe. PLoS Pathog. 2011;7:e1002304. doi: 10.1371/journal.ppat.1002304.
    1. Sanjuán R. Quasispecies. In: Mahy BWJ, van Regenmortel MHV, editors. Desk encyclopedia of general virology. Oxford: Elsevier; 2009. pp. 42–48.
    1. Swanepoel R, Smit SB, Rollin PE, Formenty P, Leman PA, Kemp A, Burt FJ, Grobbelaar AA, Croft J, Bausch DG, Zeller H, Leirs H, Braack LE, Libande ML, Zaki S, Nichol ST, Ksiazek TG, Paweska JT. Studies of reservoir hosts for Marburg virus. Emerg Infect Dis. 2007;13:1847–1851. doi: 10.3201/eid1312.071115.
    1. Towner JS, Sealy TK, Khristova ML, Albariño CG, Conlan S, Reeder SA, Quan P-L, Lipkin WI, Downing R, Tappero JW, Okware S, Lutwama J, Bakamutumaho B, Kayiwa J, Comer JA, Rollin PE, Ksiazek TG, Nichol ST. Newly discovered Ebola virus associated with hemorrhagic fever outbreak in Uganda. PLoS Pathog. 2008;4:e1000212. doi: 10.1371/journal.ppat.1000212.
    1. Towner JS, Amman BR, Sealy TK, Carroll SA, Comer JA, Kemp A, Swanepoel R, Paddock CD, Balinandi S, Khristova ML, Formenty PB, Albarino CG, Miller DM, Reed ZD, Kayiwa JT, Mills JN, Cannon DL, Greer PW, Byaruhanga E, Farnon EC, Atimnedi P, Okware S, Katongole-Mbidde E, Downing R, Tappero JW, Zaki SR, Ksiazek TG, Nichol ST, Rollin PE. Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Pathog. 2009;5:e1000536. doi: 10.1371/journal.ppat.1000536.
    1. Van Regenmortel MH, Burke DS, Calisher CH, Dietzgen RG, Fauquet CM, Ghabrial SA, Jahrling PB, Johnson KM, Holbrook MR, Horzinek MC, Keil GM, Kuhn JH, Mahy BW, Martelli GP, Pringle C, Rybicki EP, Skern T, Tesh RB, Wahl-Jensen V, Walker PJ, Weaver SC. A proposal to change existing virus species names to non-Latinized binomials. Arch Virol. 2010;155:1909–1919. doi: 10.1007/s00705-010-0831-9.
    1. van Regenmortel MHV. Viruses are real, virus species are man-made taxonomic constructions. Arch Virol. 2003;148:2481–2488. doi: 10.1007/s00705-003-0246-y.
    1. van Regenmortel MHV. Virologists, taxonomy and the demands of logic. Arch Virol. 2006;151:1251–1255. doi: 10.1007/s00705-006-0786-z.
    1. van Regenmortel MHV. Virus species and virus identification: past and current controversies. Infect Genet Evol. 2007;7:133–144. doi: 10.1016/j.meegid.2006.04.002.
    1. van Regenmortel MHV. Virus species. In: Tibayrenc M, editor. Genetics and evolution of infectious diseases. Oxford: Elsevier; 2010. pp. 3–19.
    1. Voevodin A, Marx PA. Frag-virus: a new term to distinguish presumptive viruses known primarily from sequence data. Virol J. 2008;5:34. doi: 10.1186/1743-422X-5-34.
    1. Wittmann TJ, Biek R, Hassanin A, Rouquet P, Reed P, Yaba P, Pourrut X, Real LA, Gonzalez JP, Leroy EM. Isolates of Zaire Ebola virus (sic) from wild apes reveal genetic lineage and recombinants. Proc Natl Acad Sci USA. 2007;104:17123–17127. doi: 10.1073/pnas.0704076104.
    1. World Health Organization Expert Committee on Influenza, first report. World Health Organ Tech Rep Ser. 1953;6:1–32.
    1. World Health Organization A revised system of nomenclature for influenza viruses. Bull World Health Organ. 1971;45:119–124.
    1. World Health Organization A revised system of influenza virus nomenclature—a report of the WHO study group on classification. Virology. 1972;47:854–856. doi: 10.1016/0042-6822(72)90580-6.
    1. World Health Organization Réexamen de la nomenclature des virus grippaux A: mémorandum OMS. Bull World Health Organ. 1979;57:611–617.

Source: PubMed

3
Subscribe