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Taxonomy of the family Arenaviridae and the order Bunyavirales: update 2018

Abstract

In 2018, the family Arenaviridae was expanded by inclusion of 1 new genus and 5 novel species. At the same time, the recently established order Bunyavirales was expanded by 3 species. This article presents the updated taxonomy of the family Arenaviridae and the order Bunyavirales as now accepted by the International Committee on Taxonomy of Viruses (ICTV) and summarizes additional taxonomic proposals that may affect the order in the near future.

Introduction

The family Arenaviridae was established in 1976 to accommodate predominantly murid viruses with bisegmented, ambisense single-stranded RNA genomes that form enveloped particles with a “sandy” appearance [7]. Until recently, the family was monogeneric, including the single genus Arenavirus, with a steadily increasing number of species. The taxonomy of the family was substantially amended and emended [22] following the discovery of several distinct arenaviruses in alethinophidian snakes [4, 10, 24]. In particular, the genus Arenavirus was renamed Mammarenavirus, and a second genus, Reptarenavirus, was established in 2014 for several of the newly discovered snake viruses. A non-Linnean binomial species nomenclature was adopted for the entire family Arenaviridae [22] (ICTV TaxoProps [taxonomic proposals] 2014.011a-dV and 2014.012aV). Since then, the genus Mammarenavirus has been extended by 8 species for novel murid viruses discovered in Africa and Asia [3, 8, 11, 15, 21, 25] (TaxoProps 2014.013aV.A.v3.Mammarenavirus_2sp, 2015.001aM, 2016.014aM and 2016.019aM.A.v2.Mammarenavirus_sp).

The order Bunyavirales was established in 2017 to accommodate related viruses with segmented, linear, single-stranded, negative-sense or ambisense RNA genomes distributed among nine families (TaxoProp 2016.030a-vM). In particular, the then existing family Bunyaviridae was elevated to the rank of order. The three established bunyaviral genera Hantavirus, Nairovirus, and Tospovirus were renamed Orthohantavirus, Orthonairovirus, and Orthotospovirus and included in the newly established families Hantaviridae, Nairoviridae, and Tospoviridae, respectively (TaxoProp 2016.030a-vM). The genus Orthonairovirus was expanded by five species [13] (TaxoProp 2016.026a,bM). The family Peribunyaviridae was created to include the established bunyaviral genus Orthobunyavirus and a new genus, Herbevirus, for bunyaviruses discovered in invertebrates [14, 17] (TaxoProps 2016.024a-dM and 2016.030a-vM). The family Phenuiviridae was created to accommodate the established bunyaviral genus Phlebovirus, the previously “free-floating” plant virus genus Tenuivirus, and two new genera, Goukovirus and Phasivirus, for novel invertebrate bunyaviruses [16] (TaxoProps 2016.022a-dM and 2016.027a-dM). Three new families, Feraviridae, Jonviridae, and Phasmaviridae, were established for newly discovered invertebrate bunyaviruses [2, 14, 18] (TaxoProps 2016.021a-dM, 2016.025a-dM and 2016.028a-dM). In addition, the family Fimoviridae was created to accommodate the previously “free-floating” plant virus genus Emaravirus, which was expanded by three species for newly discovered plant viruses [5, 6, 26] (TaxoProps 2016.016aP, 2016.017aP, 2016.018aP, and 2016.030a-vM). Finally, a non-Linnean binomial species nomenclature was adopted for the entire family (TaxoProps 2016.020aM, 2016.023a-cM, 2016.026a,bM, 2016.029aM.A.v2.Tenuivirus_spren, and 2016.030a-vM).

After the establishment of the order Bunyavirales, the ICTV Study Groups responsible for the taxonomy of Arenaviridae and Bunyavirales assigned unclassified viruses to existing or novel taxa and continued streamlining order nomenclature in collaboration with other virus experts. Here we present the changes to both taxa that were proposed via official TaxoProps at http://www.ictvonline.org/ in 2017 and that were accepted by the ICTV Executive Committee. These changes are official ICTV taxonomy as of March 2018.

Family Arenaviridae

Taxonomic changes at the family rank

In 2018, the family was extended by addition of a novel genus, Hartmanivirus, for Haartman Institute snake virus (HISV) isolated from a captive boa constrictor in Finland [9, 10] (TaxoProp 2017.001M.A.v1.Hartmanivirus.zip). The genus Mammarenavirus was extended by addition of two novel species for Ryukyo virus (RYKV) and souris virus (SOUV) discovered in mice in China and Cameroon, respectively (TaxoProps 2017.002M.A.v2.Mammarenavirus_sp and 2017.003M.A.v1.Mammarenavirus_sp). Five mammarenavirus species were renamed due to the ICTV decision to disallow diacritic marks in taxon names (TaxoProp 2017.001G.A.v2.43spren): Amaparí mammarenavirus, Junín mammarenavirus, Paraná mammarenavirus, Pichindé mammarenavirus, and Sabiá mammarenavirus were renamed Serra do Navio mammarenavirus, Argentinian mammarenavirus, Paraguayan mammarenavirus, Cali mammarenavirus, and Brazilian mammarenavirus, respectively, whereas the member virus names remained unchanged (TaxoProp 2017.001G.A.v2.43spren). Finally, the three reptarenavirus species names Alethinophid 1 reptarenavirus, Alethinophid 2 reptarenavirus, and Alethinophid 3 reptarenavirus were renamed Golden reptarenavirus, California reptarenavirus, and Rotterdam reptarenavirus. Two new reptarenavirus species were created for tavallinen suomalainen mies virus 2 (TSMV-2) and University of Giessen viruses 1–3 (UGV-1–3) discovered in captive boa constrictors; several newly sequenced reptarenaviruses were assigned to existing species [9] (TaxoProp 2017.015M.A.v1.Reptarenavirus_2sp3ren).

Order Bunyavirales

Taxonomic changes at the order rank

In 2018, no changes were made at the order rank.

Taxonomic changes at the family rank

Feraviridae

In 2018, no changes were made at the family rank.

Fimoviridae

In 2018, no changes were made at the family rank.

Hantaviridae

In 2018, no changes were made at the family rank.

Jonviridae

In 2018, no changes were made at the family rank.

Nairoviridae

The family Nairoviridae was expanded in 2018 by addition of two new species for the long-known but previously unsequenced Artashat virus (ARTSV) and Chim virus (CHIMV), both originally isolated from ticks. In addition, the species Burana orthonairovirus was renamed Tamdy orthonairovirus to better reflect the discovery history of species members, and several newly sequenced nairoviruses were classified into existing species [1] (TaxoProp 2017.008M.A.v1.Orthonairovirus_2sp1ren).

Peribunyaviridae

The family Peribunyaviridae was expanded in 2018 by addition of a novel species for Wolkberg virus (WBV) discovered in wingless bat flies (Eucampsipoda africana) in South Africa [12] (TaxoProp 2017.007M.A.v1.Orthobunyavirus_sp).

Phasmaviridae

In 2018, no changes were made at the family rank.

Phenuiviridae

In 2018, no changes were made at the family rank.

Tospoviridae

In 2018, no changes were made at the family rank.

Outlook

The taxonomy of viruses of the family Arenaviridae and the order Mononegavirales remains in flux, and additional important changes are likely forthcoming. Indeed, in 2017, two additional taxonomic proposals that would affect the family Arenaviridae and the order Mononegavirales were debated during the most recent ICTV EC meeting in Singapore. TaxoProp 2017.006M.U.v2.Negarnaviricota proposes the

  • establishment of a phylum for negative-sense RNA viruses that is subdivided into two subphyla; and

  • establishment of a class including the order Bunyavirales, to be assigned to one of the subphyla.

TaxoProp 2017.012M.U.v2.Bunyavirales_rev proposes

  • dissolution of the families Feraviridae, Jonviridae, and Tospoviridae and absorption of their genera into remaining families;

  • the creation of three new bunyaviral families for novel invertebrate viruses [19, 20, 23];

  • the inclusion of the family Arenaviridae in the order; and

  • the creation of 19 new bunyaviral genera. These genera are planned to accommodate novel, mostly invertebrate, viruses [14, 23], but some of them are deemed necessary for reclassification of certain hantaviruses and phleboviruses.

These two proposals failed to find unanimous approval at a final ICTV EC vote in fall of 2017 and were deferred to the 2018 ICTV EC meeting, at which a simple majority vote would suffice for approval of the original proposals.

Summary

Summaries of the current, ICTV-accepted taxonomies of the family Arenaviridae and the order Bunyavirales are presented in Tables 1 and 2, respectively. These tables also include corrections and updates in virus name or abbreviation spelling.

Table 1 ICTV-accepted taxonomy of the family Arenaviridae as of 2018. Listed are all arenaviruses that have been classified into species
Table 2 ICTV-accepted taxonomy of the order Bunyavirales as of 2018. Listed are all bunyaviruses that have been classified into species

References

  1. 1.

    Alkhovsky SV, Lvov DK, Shchetinin AM, Deriabin PG, Shchelkanov MY, Aristova VA, Morozova TN, Gitelman AK, Palacios GF, Kuhn JH (2017) Complete genome coding sequences of Artashat, Burana, Caspiy, Chim, Geran, Tamdy, and Uzun-Agach viruses (Bunyavirales: Nairoviridae: Orthonairovirus). Genome Announc 5:e01098-01017

    Article  Google Scholar 

  2. 2.

    Ballinger MJ, Bruenn JA, Hay J, Czechowski D, Taylor DJ (2014) Discovery and evolution of bunyavirids in arctic phantom midges and ancient bunyavirid-like sequences in insect genomes. J Virol 88:8783–8794

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. 3.

    Blasdell KR, Duong V, Eloit M, Chretien F, Ly S, Hul V, Deubel V, Morand S, Buchy P (2016) Evidence of human infection by a new mammarena virus endemic to Southeastern Asia. Elife 5:e13135

    Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Bodewes R, Kik MJL, Raj VS, Schapendonk CME, Haagmans BL, Smits SL, Osterhaus ADME (2013) Detection of novel divergent arenaviruses in boid snakes with inclusion body disease in The Netherlands. J Gen Virol 94:1206–1210

    Article  PubMed  CAS  Google Scholar 

  5. 5.

    Di Bello PL, Laney AG, Druciarek T, Ho T, Gergerich RC, Keller KE, Martin RR, Tzanetakis IE (2016) A novel emaravirus is associated with redbud yellow ringspot disease. Virus Res 222:41–47

    Article  PubMed  CAS  Google Scholar 

  6. 6.

    Elbeaino T, Digiaro M, Uppala M, Sudini H (2015) Deep sequencing of dsRNAs recovered from mosaic-diseased pigeonpea reveals the presence of a novel emaravirus: pigeonpea sterility mosaic virus 2. Arch Virol 160:2019–2029

    Article  PubMed  CAS  Google Scholar 

  7. 7.

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

    Article  PubMed  CAS  Google Scholar 

  8. 8.

    Gryseels S, Rieger T, Oestereich L, Cuypers B, Borremans B, Makundi R, Leirs H, Günther S, Goüy de Bellocq J (2015) Gairo virus, a novel arenavirus of the widespread Mastomys natalensis: genetically divergent, but ecologically similar to Lassa and Morogoro viruses. Virology 476:249–256

    Article  PubMed  CAS  Google Scholar 

  9. 9.

    Hepojoki J, Salmenperä P, Sironen T, Hetzel U, Korzyukov Y, Kipar A, Vapalahti O (2015) Arenavirus coinfections are common in snakes with boid inclusion body disease. J Virol 89:8657–8660

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. 10.

    Hetzel U, Sironen T, Laurinmäki P, Liljeroos L, Patjas A, Henttonen H, Vaheri A, Artelt A, Kipar A, Butcher SJ, Vapalahti O, Hepojoki J (2013) Isolation, identification, and characterization of novel arenaviruses, the etiological agents of boid inclusion body disease. J Virol 87:10918–10935

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. 11.

    Ishii A, Thomas Y, Moonga L, Nakamura I, Ohnuma A, Hang’ombe BM, Takada A, Mweene AS, Sawa H (2012) Molecular surveillance and phylogenetic analysis of Old World arenaviruses in Zambia. J Gen Virol 93:2247–2251

    Article  PubMed  CAS  Google Scholar 

  12. 12.

    Jansen van Vuren P, Wiley MR, Palacios G, Storm N, Markotter W, Birkhead M, Kemp A, Paweska JT (2017) Isolation of a novel orthobunyavirus from bat flies (Eucampsipoda africana). J Gen Virol 98:935–945

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. 13.

    Kuhn JH, Wiley MR, Rodriguez SE, Bào Y, Prieto K, Travassos da Rosa APA, Guzman H, Savji N, Ladner JT, Tesh RB, Wada J, Jahrling PB, Bente DA, Palacios G (2016) Genomic characterization of the genus Nairovirus (family Bunyaviridae). Viruses 8:164

    Article  PubMed Central  CAS  Google Scholar 

  14. 14.

    Li C-X, Shi M, Tian J-H, Lin X-D, Kang Y-J, Chen L-J, Qin X-C, Xu J, Holmes EC, Zhang Y-Z (2015) Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. Elife 4:e05378

    PubMed Central  Article  Google Scholar 

  15. 15.

    Li K, Lin X-D, Wang W, Shi M, Guo W-P, Zhang X-H, Xing J-G, He J-R, Wang K, Li M-H, Cao J-H, Jiang M-L, Holmes EC, Zhang Y-Z (2015) Isolation and characterization of a novel arenavirus harbored by rodents and shrews in Zhejiang province, China. Virology 476:37–42

    Article  PubMed  CAS  Google Scholar 

  16. 16.

    Marklewitz M, Handrick S, Grasse W, Kurth A, Lukashev A, Drosten C, Ellerbrok H, Leendertz FH, Pauli G, Junglen S (2011) Gouléako virus isolated from West African mosquitoes constitutes a proposed novel genus in the family Bunyaviridae. J Virol 85:9227–9234

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. 17.

    Marklewitz M, Zirkel F, Rwego IB, Heidemann H, Trippner P, Kurth A, Kallies R, Briese T, Lipkin WI, Drosten C, Gillespie TR, Junglen S (2013) Discovery of a unique novel clade of mosquito-associated bunyaviruses. J Virol 87:12850–12865

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. 18.

    Marklewitz M, Zirkel F, Kurth A, Drosten C, Junglen S (2015) Evolutionary and phenotypic analysis of live virus isolates suggests arthropod origin of a pathogenic RNA virus family. Proc Natl Acad Sci USA 112:7536–7541

    Article  PubMed  CAS  Google Scholar 

  19. 19.

    Marzano S-YL, Domier LL (2016) Novel mycoviruses discovered from metatranscriptomics survey of soybean phyllosphere phytobiomes. Virus Res 213:332–342

    Article  PubMed  CAS  Google Scholar 

  20. 20.

    Marzano S-YL, Nelson BD, Ajayi-Oyetunde O, Bradley CA, Hughes TJ, Hartman GL, Eastburn DM, Domier LL (2016) Identification of diverse mycoviruses through metatranscriptomics characterization of the viromes of five major fungal plant pathogens. J Virol 90:6846–6863

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. 21.

    Palacios G, Savji N, Hui J, Travassos da Rosa A, Popov V, Briese T, Tesh R, Lipkin WI (2010) Genomic and phylogenetic characterization of Merino Walk virus, a novel arenavirus isolated in South Africa. J Gen Virol 91:1315–1324

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. 22.

    Radoshitzky SR, Bào Y, Buchmeier MJ, Charrel RN, Clawson AN, Clegg CS, DeRisi JL, Emonet S, Gonzalez J-P, Kuhn JH, Lukashevich IS, Peters CJ, Romanowski V, Salvato MS, Stenglein MD, de la Torre JC (2015) Past, present, and future of arenavirus taxonomy. Arch Virol 160:1851–1874

    Article  PubMed  CAS  Google Scholar 

  23. 23.

    Shi M, Lin X-D, Tian J-H, Chen L-J, Chen X, Li C-X, Qin X-C, Li J, Cao J-P, Eden J-S, Buchmann J, Wang W, Xu J, Holmes EC, Zhang Y-Z (2016) Redefining the invertebrate RNA virosphere. Nature 540:539–543

    Article  CAS  Google Scholar 

  24. 24.

    Stenglein MD, Sanders C, Kistler AL, Ruby JG, Franco JY, Reavill DR, Dunker F, DeRisi JL (2012) Identification, characterization, and in vitro culture of highly divergent arenaviruses from boa constrictors and annulated tree boas: candidate etiological agents for snake inclusion body disease. MBio 3:e00180-00112

    Article  CAS  Google Scholar 

  25. 25.

    Witkowski PT, Kallies R, Hoveka J, Auste B, Ithete NL, Šoltys K, Szemes T, Drosten C, Preiser W, Klempa B, Mfune JKE, Kruger DH (2015) Novel arenavirus isolates from Namaqua rock mice, Namibia, Southern Africa. Emerg Infect Dis 21:1213–1216

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. 26.

    Zheng Y, Navarro B, Wang G, Wang Y, Yang Z, Xu W, Zhu C, Wang L, Di Serio F, Hong N (2017) Actinidia chlorotic ringspot-associated virus: a novel emaravirus infecting kiwifruit plants. Mol Plant Pathol 18:569–581

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Laura Bollinger (NIH/NIAID Integrated Research Facility at Fort Detrick, Frederick, MD, USA) and F. Murilo Zerbini (BIOAGRO, Universidade Federal de Viçosa, Viçosa, Brazil) for critically editing the manuscript.

Funding

This work was supported in part through Battelle Memorial Institute’s prime contract with the US National Institute of Allergy and Infectious Diseases (NIAID) under Contract No. HHSN272200700016I (J.H.K.). This work was also funded in part by National Institutes of Health (NIH) contract HHSN272201000040I/HHSN27200004/D04 and Grant R24AI120942 (N.V., R.B.T.), intramural funds of the US Department of Health and Human Services to the US National Library of Medicine (E.V.K. and Y.I.W.), and the 100-Talent Program of the Chinese Academy of Sciences, the National Key R&D Program of China (2016YFE0206600) and the International Union of Biological Sciences (Y.B.).

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Correspondence to Jens H. Kuhn.

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Michael J. Buchmeier, Rémi N. Charrel, Christopher S. Clegg, Juan Carlos de la Torre, Joseph L. DeRisi, Jean-Paul J. Gonzalez, S. Lukashevich, Clarence J. Peters, Sheli R. Radoshitzky, Víctor Romanowski, Maria S. Salvato and Jens H. Kuhn were the members of the 2014–2017 International Committee on Taxonomy of Viruses (ICTV) Arenaviridae Study Group.

Piet Maes, Sergey V. Alkhovsky, Martin Beer, Thomas Briese, Charles H. Calisher, Rémi N. Charrel, Hideki Ebihara, Rakesh K. Jain, Amy J. Lambert, Márcio Roberto Teixeira Nunes, Alexander Plyusnin, Connie Schmaljohn, Robert B. Tesh, Shyi-Dong Yeh and Jens H. Kuhn were the members of the 2014–2017 ICTV Bunyaviridae Study Group.

Michele Digiaro, Toufic Elbeaino, Giovanni P. Martelli, Nicole Mielke-Ehret and Hans-Peter Mühlbach were the members of the 2014–2017 ICTV Emaravirus Study Group.

Il Ryong Choi, Anne-Lise Haenni, Miranda Gilda Jonson, Takahide Sasaya, Yukio Shirako, Tàiyún Wèi and Xueping Zhou were the members of the 2014–2017 ICTV Tenuivirus Study Group.

Stuart Siddell was the Chair of the 2014–2017 ICTV Animal dsRNA and ssRNA-Viruses Subcommittee.

Hélène Sanfaçon was the Chair of the 2014–2017 ICTV Plant Viruses Subcommittee.

Handling Editor: Sead Sabanadzovic.

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Maes, P., Alkhovsky, S.V., Bào, Y. et al. Taxonomy of the family Arenaviridae and the order Bunyavirales: update 2018. Arch Virol 163, 2295–2310 (2018). https://doi.org/10.1007/s00705-018-3843-5

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