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01-03-2016 | Virology Division News

Reorganization and expansion of the nidoviral family Arteriviridae

Published in: Archives of Virology | Issue 3/2016

Abstract

The family Arteriviridae presently includes a single genus Arterivirus. This genus includes four species as the taxonomic homes for equine arteritis virus (EAV), lactate dehydrogenase-elevating virus (LDV), porcine respiratory and reproductive syndrome virus (PRRSV), and simian hemorrhagic fever virus (SHFV), respectively. A revision of this classification is urgently needed to accommodate the recent description of eleven highly divergent simian arteriviruses in diverse African nonhuman primates, one novel arterivirus in an African forest giant pouched rat, and a novel arterivirus in common brushtails in New Zealand. In addition, the current arterivirus nomenclature is not in accordance with the most recent version of the International Code of Virus Classification and Nomenclature. Here we outline an updated, amended, and improved arterivirus taxonomy based on current data. Taxon-specific sequence cut-offs are established relying on a newly established open reading frame 1b phylogeny and pairwise sequence comparison (PASC) of coding-complete arterivirus genomes. As a result, the current genus Arterivirus is replaced by five genera: Equartevirus (for EAV), Rodartevirus (LDV + PRRSV), Simartevirus (SHFV + simian arteriviruses), Nesartevirus (for the arterivirus from forest giant pouched rats), and Dipartevirus (common brushtail arterivirus). The current species Porcine reproductive and respiratory syndrome virus is divided into two species to accommodate the clear divergence of the European and American “types” of PRRSV, both of which now receive virus status. The current species Simian hemorrhagic fever virus is divided into nine species to accommodate the twelve known simian arteriviruses. Non-Latinized binomial species names are introduced to replace all current species names to clearly differentiate them from virus names, which remain largely unchanged.

Abascal F, Zardoya R, Telford MJ (2010) TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res 38:W7–13PubMedCentralCrossRefPubMed

Adams MJ, Carstens EB (2012) Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2012). Arch Virol 157:1411–1422CrossRefPubMed

Adams MJ, King AM, Carstens EB (2013) Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2013). Arch Virol 158:2023–2030CrossRefPubMed

Adams MJ, Lefkowitz EJ, King AM, Carstens EB (2013) Recently agreed changes to the International Code of Virus Classification and Nomenclature. Arch Virol 158:2633–2639CrossRefPubMed

Adams MJ, Carstens EB (2014) Changes to the Statutes and Subcommittees of the International Committee on Taxonomy of Viruses (2014). Arch Virol 159:2829–2830CrossRefPubMed

Adams MJ, Lefkowitz EJ, King AM, Carstens EB (2014) Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2014). Arch Virol 159:2831–2841CrossRefPubMed

Adams MJ, Lefkowitz EJ, King AM, Bamford DH, Breitbart M, Davison AJ, Ghabrial SA, Gorbalenya AE, Knowles NJ, Krell P, Lavigne R, Prangishvili D, Sanfaçon H, Siddell SG, Simmonds P, Carstens EB (2015) Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2015). Arch Virol 160:1837–1850CrossRefPubMed

Anthony SJ, Epstein JH, Murray KA, Navarrete-Macias I, Zambrana-Torrelio CM, Solovyov A, Ojeda-Flores R, Arrigo NC, Islam A, Ali Khan S, Hosseini P, Bogich TL, Olival KJ, Sanchez-Leon MD, Karesh WB, Goldstein T, Luby SP, Morse SS, Mazet JA, Daszak P, Lipkin WI (2013) A strategy to estimate unknown viral diversity in mammals. MBio 4:e00598–00513CrossRef

Bailey AL, Lauck M, Sibley SD, Pecotte J, Rice K, Weny G, Tumukunde A, Hyeroba D, Greene J, Correll M, Gleicher M, Friedrich TC, Jahrling PB, Kuhn JH, Goldberg TL, Rogers J, O’Connor DH (2014) Two novel simian arteriviruses in captive and wild baboons (Papio spp.). J Virol 88:13231–13239PubMedCentralCrossRefPubMed

10.

Bailey AL, Lauck M, Weiler A, Sibley SD, Dinis JM, Bergman Z, Nelson CW, Correll M, Gleicher M, Hyeroba D, Tumukunde A, Weny G, Chapman C, Kuhn JH, Hughes AL, Friedrich TC, Goldberg TL, O’Connor DH (2014) High genetic diversity and adaptive potential of two simian hemorrhagic fever viruses in a wild primate population. PLoS One 9:e90714PubMedCentralCrossRefPubMed

11.

Bao Y, Chetvernin V, Tatusova T (2014) Improvements to pairwise sequence comparison (PASC): a genome-based web tool for virus classification. Arch Virol 159:3293–3304PubMedCentralCrossRefPubMed

12.

Benfield DA, Nelson E, Collins JE, Harris L, Goyal SM, Robison D, Christianson WT, Morrison RB, Gorcyca D, Chladek D (1992) Characterization of swine infertility and respiratory syndrome (SIRS) virus (isolate ATCC VR-2332). J Vet Diagn Invest 4:127–133CrossRefPubMed

13.

Breitbart M, Rohwer F (2005) Here a virus, there a virus, everywhere the same virus? Trends Microbiol 13:278–284CrossRefPubMed

14.

Brinton MA, Godeny EK, Horzinek MC, Meulenberg JJM, Murtaugh MP, Plagemann PG, Snijder EJ (2000) Family Arteriviridae. In: van Regenmortel MHV, Fauquet CM, Bishop DHL, Carstens EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeoch DJ, Pringle CR, Wickner RB (eds) Virus taxonomy—seventh report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, pp 851–857

15.

Bryans JT, Crowe ME, Doll ER, McCollum WH (1957) Isolation of a filterable agent causing arteritis of horses and abortion by mares; its differentiation from the equine abortion (influenza) virus. Cornell Vet 47:3–41PubMed

16.

Calisher CH, Mahy BW (2003) Taxonomy: get it right or leave it alone. Am J Trop Med Hyg 68:505–506PubMed

17.

Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552CrossRefPubMed

18.

Cavanagh D, Brain DA, Brinton MA, Enjuanes L, Holmes KV, Horzinek MC, Lai MMC, Laude H, Plagemann PGW, Siddell SG, Spaan WJM, Taguchi F, Talbot PJ (1995) Genus Arterivirus. In: Murphy FA, Fauquet CM, Bishop DHL, Ghabrial SA, Jarvis AW, Martelli GP, Mayo MA, Summers MD (eds) Virus taxonomy—sixth report of the International Committee on Taxonomy of Viruses. Springer, Vienna, pp 412–414

19.

Collins JE, Benfield DA, Christianson WT, Harris L, Hennings JC, Shaw DP, Goyal SM, McCullough S, Morrison RB, Joo HS et al (1992) Isolation of swine infertility and respiratory syndrome virus (isolate ATCC VR-2332) in North America and experimental reproduction of the disease in gnotobiotic pigs. J Vet Diagn Invest 4:117–126CrossRefPubMed

20.

de Vries AA, Chirnside ED, Bredenbeek PJ, Gravestein LA, Horzinek MC, Spaan WJ (1990) All subgenomic mRNAs of equine arteritis virus contain a common leader sequence. Nucleic Acids Res 18:3241–3247PubMedCentralCrossRefPubMed

21.

den Boon JA, Snijder EJ, Chirnside ED, de Vries AA, Horzinek MC, Spaan WJ (1991) Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily. J Virol 65:2910–2920

22.

Dunowska M, Biggs PJ, Zheng T, Perrott MR (2012) Identification of a novel nidovirus associated with a neurological disease of the Australian brushtail possum (Trichosurus vulpecula). Vet Microbiol 156:418–424CrossRefPubMed

23.

Enjuanes L, Spaan W, Snijder E, Cavanagh D (2000) Order Nidovirales. In: van Regenmortel MHV, Fauquet CM, Bishop DHL, Carstens EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeoch DJ, Pringle CR, Wickner RB (eds) Virus taxonomy—seventh report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, California, USA, pp 827–834

24.

Faaberg KS, Balasuriya UB, Brinton MA, Gorbalenya AE, Leung FC-C, Nauwynck H, Snijder EJ, Stadejek T, Yang H, Yoo D (2011) Family Arteriviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy—ninth report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, London, pp 796–805

25.

Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRef

26.

Fenner F (1976) Classification and nomenclature of viruses. Second report of the International Committee on Taxonomy of Viruses. Intervirology 7:1–115CrossRefPubMed

27.

Giles JC, Perrott MR, Dunowska M (2015) Primary possum macrophage cultures support the growth of a nidovirus associated with wobbly possum disease. J Virol Methods 222:66–71CrossRefPubMed

28.

Godeny EK, de Vries AA, Wang XC, Smith SL, de Groot RJ (1998) Identification of the leader-body junctions for the viral subgenomic mRNAs and organization of the simian hemorrhagic fever virus genome: evidence for gene duplication during arterivirus evolution. J Virol 72:862–867PubMedCentralPubMed

29.

Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066PubMedCentralCrossRefPubMed

30.

King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (2011) The International Code of Virus Classification and Nomenclature. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy—ninth report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, London, pp 1273–1277

31.

Kuhn JH, Jahrling PB (2010) Clarification and guidance on the proper usage of virus and virus species names. Arch Virol 155:445–453PubMedCentralCrossRefPubMed

32.

Kuhn JH, Bao Y, Bavari S, Becker S, Bradfute S, Brister JR, Bukreyev AA, Caì Y, Chandran K, Davey RA, Dolnik O, Dye JM, Enterlein S, Gonzalez JP, Formenty P, Freiberg AN, Hensley LE, Honko AN, Ignatyev GM, Jahrling PB, Johnson KM, Klenk HD, Kobinger G, Lackemeyer MG, Leroy EM, Lever MS, Lofts LL, Mühlberger E, Netesov SV, Olinger GG, Palacios G, Patterson JL, Paweska JT, Pitt L, Radoshitzky SR, Ryabchikova EI, Saphire EO, Shestopalov AM, Smither SJ, Sullivan NJ, Swanepoel R, Takada A, Towner JS, van der Groen G, Volchkov VE, Wahl-Jensen V, Warren TK, Warfield KL, Weidmann M, Nichol ST (2013) Virus nomenclature below the species level: a standardized nomenclature for laboratory animal-adapted strains and variants of viruses assigned to the family Filoviridae. Arch Virol 158:1425–1432PubMedCentralCrossRefPubMed

33.

Kuhn JH, Bao Y, Bavari S, Becker S, Bradfute S, Brister JR, Bukreyev AA, Chandran K, Davey RA, Dolnik O, Dye JM, Enterlein S, Hensley LE, Honko AN, Jahrling PB, Johnson KM, Kobinger G, Leroy EM, Lever MS, Mühlberger E, Netesov SV, Olinger GG, Palacios G, Patterson JL, Paweska JT, Pitt L, Radoshitzky SR, Saphire EO, Smither SJ, Swanepoel R, Towner JS, van der Groen G, Volchkov VE, Wahl-Jensen V, Warren TK, Weidmann M, Nichol ST (2013) Virus nomenclature below the species level: a standardized nomenclature for natural variants of viruses assigned to the family Filoviridae. Arch Virol 158:301–311PubMedCentralCrossRefPubMed

34.

Kuhn JH, Bào Y, Bavari S, Becker S, Bradfute S, Brauburger K, Rodney Brister J, Bukreyev AA, Caì Y, Chandran K, Davey RA, Dolnik O, Dye JM, Enterlein S, Gonzalez JP, Formenty P, Freiberg AN, Hensley LE, Hoenen T, Honko AN, Ignatyev GM, Jahrling PB, Johnson KM, Klenk HD, Kobinger G, Lackemeyer MG, Leroy EM, Lever MS, Mühlberger E, Netesov SV, Olinger GG, Palacios G, Patterson JL, Paweska JT, Pitt L, Radoshitzky SR, Ryabchikova EI, Saphire EO, Shestopalov AM, Smither SJ, Sullivan NJ, Swanepoel R, Takada A, Towner JS, van der Groen G, Volchkov VE, Volchkova VA, Wahl-Jensen V, Warren TK, Warfield KL, Weidmann M, Nichol ST (2014) Virus nomenclature below the species level: a standardized nomenclature for filovirus strains and variants rescued from cDNA. Arch Virol 159:1229–1237PubMedCentralPubMed

35.

Lauck M, Hyeroba D, Tumukunde A, Weny G, Lank SM, Chapman CA, O’Connor DH, Friedrich TC, Goldberg TL (2011) Novel, divergent simian hemorrhagic fever viruses in a wild Ugandan red colobus monkey discovered using direct pyrosequencing. PLoS One 6:e19056PubMedCentralCrossRefPubMed

36.

Lauck M, Sibley SD, Hyeroba D, Tumukunde A, Weny G, Chapman CA, Ting N, Switzer WM, Kuhn JH, Friedrich TC, O’Connor DH, Goldberg TL (2013) Exceptional simian hemorrhagic fever virus diversity in a wild African primate community. J Virol 87:688–691PubMedCentralCrossRefPubMed

37.

Lauck M, Alkhovsky SV, Bao Y, Bailey AL, Shevtsova ZV, Shchetinin AM, Vishnevskaya TV, Lackemeyer MG, Postnikova E, Mazur S, Wada J, Radoshitzky SR, Friedrich TC, Lapin BA, Deriabin PG, Jahrling PB, Goldberg TL, O’Connor DH, Kuhn JH (2015) Historical outbreaks of simian hemorrhagic fever in captive macaques were caused by distinct arteriviruses. J Virol 89:8082–8087PubMedCentralCrossRefPubMed

38.

Li CX, Shi M, Tian JH, Lin XD, Kang YJ, Chen LJ, Qin XC, Xu J, Holmes EC, Zhang YZ (2015) Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. Elife 4:e05378

39.

Matthews RE (1979) Third report of the International Committee on Taxonomy of Viruses. Classification and nomenclature of viruses. Intervirology 12:129–296CrossRefPubMed

40.

Matthews RE (1982) Classification and nomenclature of viruses. Fourth report of the International Committee on Taxonomy of Viruses. Intervirology 17:1–199CrossRef

41.

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 (2011) Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol 156:1397–1413PubMedCentralCrossRefPubMed

42.

Meredith RW, Janecka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simao TL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrick A, Westerman M, Ayoub NA, Springer MS, Murphy WJ (2011) Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science 334:521–524CrossRefPubMed

43.

Mittelholzer C, Stadejek T, Johansson I, Baule C, Ciabatti I, Hannant D, Paton D, Autorino GL, Nowotny N, Belak S (2006) Extended phylogeny of equine arteritis virus: division into new subgroups. J Vet Med B Infect Dis Vet Public Health 53:55–58CrossRefPubMed

44.

Notkins AL, Scheele C (1963) An infectious nucleic acid from the lactic dehydrogenase agent. Virology 20:640–642CrossRefPubMed

45.

Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMed

46.

Snijder EJ, Brinton MA, Faaberg KS, Godeny EK, Gorbalenya AE, MacLachlan NJ, Mengeling WL, Plagemann PGW (2005) Family Arteriviridae. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) Virus taxonomy—eighth report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, San Diego, pp 965–974

47.

Snijder EJ, Kikkert M, Fang Y (2013) Arterivirus molecular biology and pathogenesis. J Gen Virol 94:2141–2163CrossRefPubMed

48.

Spaan WJM, den Boon JA, Bredenbeek PJ, Chirnside ED, Noten AFH, Snijder EJ, de Vries AAF, Horzinek MC (1990) Comparative and evolutionary aspects of Coronaviral, Arteriviral, and Toroviral genome structure and expression. In: Brinton MA, Heinz FX (eds) New aspects of positive-strand RNA viruses. American Society for Microbiology, Washington, DC, pp 12–19

49.

Stadejek T, Stankevicius A, Storgaard T, Oleksiewicz MB, Belak S, Drew TW, Pejsak Z (2002) Identification of radically different variants of porcine reproductive and respiratory syndrome virus in Eastern Europe: towards a common ancestor for European and American viruses. J Gen Virol 83:1861–1873CrossRefPubMed

50.

Stadejek T, Oleksiewicz MB, Potapchuk D, Podgorska K (2006) Porcine reproductive and respiratory syndrome virus strains of exceptional diversity in eastern Europe support the definition of new genetic subtypes. J Gen Virol 87:1835–1841CrossRefPubMed

51.

Strauss JH (1991) Family Togaviridae. In: Francki RIB, Fauquet CM, Knudson DL, Brown F (eds) Classification and nomenclature of viruses—fifth report of the International Committee on Taxonomy of Viruses. Springer, Vienna, pp 216–222

52.

Tauraso NM, Shelokov A, Palmer AE, Allen AM (1968) Simian hemorrhagic fever. 3. Isolation and characterization of a viral agent. Am J Trop Med Hyg 17:422–431PubMed

53.

Van Regenmortel MH (2007) Virus species and virus identification: past and current controversies. Infect Genet Evol 7:133–144CrossRefPubMed

54.

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 (2010) A proposal to change existing virus species names to non-Latinized binomials. Arch Virol 155:1909–1919CrossRefPubMed

55.

Vetten HJ, Haenni AL (2006) Taxon-specific suffixes for vernacular names. Arch Virol 151:1249–1250CrossRefPubMed

56.

Wengler G (1991) Family Flaviviridae. In: Francki RIB, Fauquet CM, Knudson DL, Brown F (eds) Classification and nomenclature of viruses—fifth report of the International Committee on Taxonomy of Viruses. Springer, Vienna, pp 223–233

57.

Wensvoort G, Terpstra C, Pol JM, ter Laak EA, Bloemraad M, de Kluyver EP, Kragten C, van Buiten L, den Besten A, Wagenaar F et al (1991) Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Vet Q 13:121–130CrossRefPubMed

58.

Wildy P (1971) Classification and nomenclature of viruses. First report of the International Committee on Nomenclature of Viruses. Karger, Basel

59.

Zeegers JJ, Van der Zeijst BA, Horzinek MC (1976) The structural proteins of equine arteritis virus. Virology 73:200–205CrossRefPubMed

60.

Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97–166

Title: Reorganization and expansion of the nidoviral family Arteriviridae
Publication date: 01-03-2016
Published in: Archives of Virology / Issue 3/2016
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI: https://doi.org/10.1007/s00705-015-2672-z

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