BACKGROUND: In the past decade, many new paramyxoviruses that do not belong to any of the seven established genera in the family Paramyxoviridae have been discovered. Amongst them are J-virus (JPV), Beilong virus (BeiPV) and Tailam virus (TlmPV), three paramyxovirus species found in rodents. Based on their similarities, it has been suggested that these viruses should compose a new genus, tentatively called 'Jeilongvirus'. RESULTS: Here we present the complete genomes of three newly discovered paramyxoviruses, one found in a bank vole (Myodes glareolus) from Slovenia and two in a single, co-infected Rungwe brush-furred rat (Lophuromys machangui) from Mozambique, that represent three new, separate species within the putative genus 'Jeilongvirus'. The genome organization of these viruses is similar to other paramyxoviruses, but like JPV, BeiPV and TlmPV, they possess an additional open reading frame, encoding a transmembrane protein, that is located between the F and G genes. As is the case for all Jeilongviruses, the G genes of the viruses described here are unusually large, and their encoded proteins are characterized by a remarkable amino acid composition pattern that is not seen in other paramyxoviruses, but resembles certain motifs found in Orthopneumovirus G proteins. CONCLUSIONS: The phylogenetic clustering of JPV, BeiPV and TlmPV with the viruses described here, as well as their shared features that set them apart from other paramyxoviruses, provide additional support for the recognition of the genus 'Jeilongvirus'.

Department of Biology Evolutionary Ecology Group University of Antwerp Universiteitsplein 1 2610 Antwerpen Belgium

Department of Microbiology and Immunology Laboratory of Clinical Virology Rega Institute for Medical Research KU Leuven University of Leuven Herestraat 49 Box 1040 BE3000 Leuven Belgium

Department of Microbiology and Immunology Laboratory of Evolutionary and Computational Virology Rega Institute for Medical Research KU Leuven University of Leuven Herestraat 49 Box 1040 BE3000 Leuven Belgium

Department of Microbiology and Immunology Laboratory of Viral Metagenomics Rega Institute for Medical Research KU Leuven University of Leuven Herestraat 49 Box 1040 BE3000 Leuven Belgium

Ecology and Evolutionary Biology Department University of Arizona 1041 E Lowell St Tucson AZ 85719 USA

Institute of Microbiology and Immunology Faculty of Medicine University of Ljubljana Zaloška 4 SI 1000 Ljubljana Slovenia

The Czech Academy of Sciences Institute of Vertebrate Biology Květná 8 603 65 Brno Czech Republic

Zobrazit více v PubMed

Samal SK. The biology of paramyxoviruses. Norfolk, UK: Caister Academic Press; 2011.

Moss WJ. Measles. Lancet. 2017;390(10111):2490–2502. doi: 10.1016/S0140-6736(17)31463-0. PubMed DOI

Rubin S, Eckhaus M, Rennick LJ, Bamford CG, Duprex WP. Molecular biology, pathogenesis and pathology of mumps virus. J Pathol. 2015;235(2):242–252. doi: 10.1002/path.4445. PubMed DOI PMC

Schomacker H, Schaap-Nutt A, Collins PL, Schmidt AC. Pathogenesis of acute respiratory illness caused by human parainfluenza viruses. Curr Opin Virol. 2012;2(3):294–299. doi: 10.1016/j.coviro.2012.02.001. PubMed DOI PMC

Escaffre O, Borisevich V, Rockx B. Pathogenesis of Hendra and Nipah virus infection in humans. J Infect Dev Ctries. 2013;7(4):308–311. doi: 10.3855/jidc.3648. PubMed DOI

Ortin J, Martin-Benito J. The RNA synthesis machinery of negative-stranded RNA viruses. Virology. 2015;479-480:532–544. doi: 10.1016/j.virol.2015.03.018. PubMed DOI

Virus Taxonomy: 2016 Release [https://talk.ictvonline.org/taxonomy/].

Alkhovsky S, Butenko A, Eremyan A, Shchetinin A. Genetic characterization of bank vole virus (BaVV), a new paramyxovirus isolated from kidneys of bank voles in Russia. Arch Virol. 2018;163(3):755–59. PubMed

Jun MH, Karabatsos N, Johnson RH. A new mouse paramyxovirus (J virus) Aust J Exp Biol Med Sci. 1977;55(6):645–647. doi: 10.1038/icb.1977.63. PubMed DOI

Li Z, Yu M, Zhang H, Magoffin DE, Jack PJ, Hyatt A, Wang HY, Wang LF. Beilong virus, a novel paramyxovirus with the largest genome of non-segmented negative-stranded RNA viruses. Virology. 2006;346(1):219–228. doi: 10.1016/j.virol.2005.10.039. PubMed DOI

Miller PJ, Boyle DB, Eaton BT, Wang LF. Full-length genome sequence of Mossman virus, a novel paramyxovirus isolated from rodents in Australia. Virology. 2003;317(2):330–344. doi: 10.1016/j.virol.2003.08.013. PubMed DOI

Renshaw RW, Glaser AL, Van Campen H, Weiland F, Dubovi EJ. Identification and phylogenetic comparison of Salem virus, a novel paramyxovirus of horses. Virology. 2000;270(2):417–429. doi: 10.1006/viro.2000.0305. PubMed DOI

Tidona CA, Kurz HW, Gelderblom HR, Darai G. Isolation and molecular characterization of a novel cytopathogenic paramyxovirus from tree shrews. Virology. 1999;258(2):425–434. doi: 10.1006/viro.1999.9693. PubMed DOI

Tikasingh ES, Jonkers AH, Spence L, Aitken TH. Nariva virus, a hitherto undescribed agent isolated from the Trinidadian rat, Zygodontomys b. Brevicauda (J. A. Allen & Chapman) Am J Trop Med Hyg. 1966;15(2):235–238. doi: 10.4269/ajtmh.1966.15.235. PubMed DOI

Woo PC, Lau SK, Wong BH, Wong AY, Poon RW, Yuen KY. Complete genome sequence of a novel paramyxovirus, Tailam virus, discovered in Sikkim rats. J Virol. 2011;85(24):13473–13474. doi: 10.1128/JVI.06356-11. PubMed DOI PMC

Shi M, Lin XD, Chen X, Tian JH, Chen LJ, Li K, Wang W, Eden JS, Shen JJ, Liu L, et al. The evolutionary history of vertebrate RNA viruses. Nature. 2018;556(7700):197–202. PubMed

Rima B, Collins P, Easton A, Fouchier R, Kurath G, Lamb RA, Lee B, Maisner A, Rota P, Wang LF. Problems of classification in the family Paramyxoviridae. Arch Virol. 2018;163(5):1395–1404. doi: 10.1007/s00705-018-3720-2. PubMed DOI PMC

Calain P, Roux L. The rule of six, a basic feature for efficient replication of Sendai virus defective interfering RNA. J Virol. 1993;67(8):4822–4830. PubMed PMC

Bao Y, Chetvernin V, Tatusova T. Improvements to pairwise sequence comparison (PASC): a genome-based web tool for virus classification. Arch Virol. 2014;159(12):3293–3304. doi: 10.1007/s00705-014-2197-x. PubMed DOI PMC

Vidal S, Curran J, Kolakofsky D. A stuttering model for paramyxovirus P mRNA editing. EMBO J. 1990;9(6):2017–2022. PubMed PMC

Li Z, Hung C, Paterson RG, Michel F, Fuentes S, Place R, Lin Y, Hogan RJ, Lamb RA, He B. Type II integral membrane protein, TM of J paramyxovirus promotes cell-to-cell fusion. Proc Natl Acad Sci U S A. 2015;112(40):12504–12509. doi: 10.1073/pnas.1509476112. PubMed DOI PMC

Wilson RL, Fuentes SM, Wang P, Taddeo EC, Klatt A, Henderson AJ, He B. Function of small hydrophobic proteins of paramyxovirus. J Virol. 2006;80(4):1700–1709. doi: 10.1128/JVI.80.4.1700-1709.2006. PubMed DOI PMC

Poehlmann S, Simmons G. Viral entry into host cells. New York, N.Y. ; Austin, Tex: Springer Science+Business Media ; Landes Bioscience; 2013.

Woo PCY, Wong AYP, Wong BHL, Lam CSF, Fan RYY, Lau SKP, Yuen KY. Comparative genome and evolutionary analysis of naturally occurring Beilong virus in brown and black rats. Infect Genet Evol. 2016;45:311–319. doi: 10.1016/j.meegid.2016.09.016. PubMed DOI

Bose S, Jardetzky TS, Lamb RA. Timing is everything: fine-tuned molecular machines orchestrate paramyxovirus entry. Virology. 2015;479-480:518–531. doi: 10.1016/j.virol.2015.02.037. PubMed DOI PMC

Chatziandreou N, Stock N, Young D, Andrejeva J, Hagmaier K, McGeoch DJ, Randall RE. Relationships and host range of human, canine, simian and porcine isolates of simian virus 5 (parainfluenza virus 5) J Gen Virol. 2004;85(Pt 10):3007–3016. doi: 10.1099/vir.0.80200-0. PubMed DOI

Lee B, Rota PA. Henipavirus: ecology, molecular virology, and pathogenesis. Heidelberg; New York: Springer; 2012.

Maganga GD, Bourgarel M, Obame Nkoghe J, N'Dilimabaka N, Drosten C, Paupy C, Morand S, Drexler JF, Leroy EM. Identification of an unclassified paramyxovirus in Coleura afra: a potential case of host specificity. PLoS One. 2014;9(12):e115588. doi: 10.1371/journal.pone.0115588. PubMed DOI PMC

Le Bayon JC, Lina B, Rosa-Calatrava M, Boivin G. Recent developments with live-attenuated recombinant paramyxovirus vaccines. Rev Med Virol. 2013;23(1):15–34. doi: 10.1002/rmv.1717. PubMed DOI

Jack PJ, Boyle DB, Eaton BT, Wang LF. The complete genome sequence of J virus reveals a unique genome structure in the family Paramyxoviridae. J Virol. 2005;79(16):10690–10700. doi: 10.1128/JVI.79.16.10690-10700.2005. PubMed DOI PMC

Jack PJ, Anderson DE, Bossart KN, Marsh GA, Yu M, Wang LF. Expression of novel genes encoded by the paramyxovirus J virus. J Gen Virol. 2008;89(Pt 6):1434–1441. doi: 10.1099/vir.0.83638-0. PubMed DOI

Wertz GW, Collins PL, Huang Y, Gruber C, Levine S, Ball LA. Nucleotide sequence of the G protein gene of human respiratory syncytial virus reveals an unusual type of viral membrane protein. Proc Natl Acad Sci U S A. 1985;82(12):4075–4079. doi: 10.1073/pnas.82.12.4075. PubMed DOI PMC

Collins PL, Melero JA. Progress in understanding and controlling respiratory syncytial virus: still crazy after all these years. Virus Res. 2011;162(1–2):80–99. doi: 10.1016/j.virusres.2011.09.020. PubMed DOI PMC

Li Z, Xu J, Patel J, Fuentes S, Lin Y, Anderson D, Sakamoto K, Wang LF, He B. Function of the small hydrophobic protein of J paramyxovirus. J Virol. 2011;85(1):32–42. doi: 10.1128/JVI.01673-10. PubMed DOI PMC

Dupinay T, Pounder KC, Ayral F, Laaberki MH, Marston DA, Lacote S, Rey C, Barbet F, Voller K, Nazaret N, et al. Detection and genetic characterization of Seoul virus from commensal brown rats in France. Virol J. 2014;11:32. doi: 10.1186/1743-422X-11-32. PubMed DOI PMC

Stang A, Korn K, Wildner O, Uberla K. Characterization of virus isolates by particle-associated nucleic acid PCR. J Clin Microbiol. 2005;43(2):716–720. doi: 10.1128/JCM.43.2.716-720.2005. PubMed DOI PMC

Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC

Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25(15):1972–1973. doi: 10.1093/bioinformatics/btp348. PubMed DOI PMC

Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33(7):1870–1874. doi: 10.1093/molbev/msw054. PubMed DOI PMC

Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29(8):1969–1973. doi: 10.1093/molbev/mss075. PubMed DOI PMC

Whelan S, Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol. 2001;18(5):691–699. doi: 10.1093/oxfordjournals.molbev.a003851. PubMed DOI

Yang Z. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol. 1994;39(3):306–314. doi: 10.1007/BF00160154. PubMed DOI

Phylogenomic Characterization of Lopma Virus and Praja Virus, Two Novel Rodent-Borne Arteriviruses

Genome Sequence of Ruloma Virus, a Novel Paramyxovirus Clustering Basally to Members of the Genus Jeilongvirus

Molecular detection and genomic characterization of diverse hepaciviruses in African rodents