Academ Virus, a Novel Hantavirus in the Siberian Mole (Talpa altaica) from Russia

Abstract

To date, six hantavirus species have been detected in moles (family Talpidae). In this report, we describe Academ virus (ACDV), a novel hantavirus harbored by the Siberian mole (Talpa altaica) in Western Siberia. Genetic analysis of the complete S-, M-, and partial L-genomic segments showed that ACDV shared a common evolutionary origin with Bruges virus, previously identified in the European mole (Talpa europaea), and is distantly related to other mole-borne hantaviruses. Co-evolution and local adaptation of genetic variants of hantaviruses and their hosts, with possible reassortment events, might have shaped the evolutionary history of ACDV.

Keywords: Hantaviridae; Russia; evolution; hantavirus; mole.

Figure 1

Map, showing the locations of the collection sites in West Siberia, Russia, where hantavirus-infected Siberian moles were captured. (1) Academgorodok, (2) Teletskoye, (3) Azhendarovo. The inset shows the geographic range of Talpa altaica (area colored in blue).

Figure 2

Phylogenetic trees generated by the Bayesian method, under the best-fit GTR+I+Γ model of evolution, based on the S-, M-, and L-genomic segments of ACDV (green, bold lettering). The phylogenetic positions of ACDV strains in Russia are shown in relationship to mole-borne hantaviruses (green): Asama orthohantavirus (ASAV N10, S: EU929072; M: EU929075; L: EU929078) from Urotrichus talpoides, Nova mobatvirus (NVAV Te34, S: KR072621, M: KR072622, L: KR072623), and Bruges orthohantavirus (BRGV BE/VieuxGenappeTE2013, S: KR072621; M: KR072622; L: KR072623 and BRGV DEWandlitzTE2013, S: MF683844; M: MF683845; L: MF683846) from Talpa europaea, Rockport orthohantavirus (RKPV MSB57412, S: HM015223; M: HM015222; L: HM015221) from Scalopus aquaticus, and Oxbow orthohantavirus (OXBV Ng1453, S: FJ5339166; M: FJ539167; L: FJ593497) from Neurotrichus gibbsii. Shrew-borne hantaviruses (red lettering) include Thottapalayam thottimvirus (TPMV VRC66412, S: AY526097, M: EU001329, L: EU001330) from Suncus murinus, Imjin thottimvirus (MJNV Cl05-11, S: EF641804; M: EF641798; L: EF641806) from Crocidura lasiura, Uluguru thottimvirus (ULUV FMNH158302, S: JX193695; M: JX193696; L: JX193697) from Myosorex geata, Kilimanjaro thottimvirus (KMJV FMNH174124, S: JX193698; M: JX193699; L: JX193700) from Myosorex zinki, Jeju orthohantavirus (JJUV SH42, S: HQ663933; M: HQ663934; L: HQ663935) from Crocidura shantungensis, Cao Bằng orthohantavirus (CBNV TC-3, S: EF543524; M: EF543526; L: EF543525) from Anourosorex squamipes, Azagny orthohantavirus (AZGV KBM15, S: JF276226; M: JF276227; L: JF276228) from Crocidura obscurior, Bowé orthohantavirus (BOWV VN1512, S: KC631782; M: KC631783; L: KC631784) from Crocidura douceti, prototype Seewis orthohantavirus (SWSV mp70, S: EF636024; M: EF636025; L: EF636026), and Altai virus (ALTV ALT302, S: MK340902; M: MK340903; L: MT648514) from Sorex araneus, Lena virus (LENV Khekhtsir-Sc67, S: MH499470; M: MH499471; L: MH499472) from Sorex caecutiens, Asikkala virus (ASIV CZ/Drahany/420/2010/Sm, S: KC880342; M: KC880345; L: KC880348) from Sorex minutus, Jemez Springs orthohantavirus (JMSV MSB144475, S: FJ593499; M: FJ593500; L: FJ593501) from Sorex monticolus, Tanganya virus (TGNV Tan826, S: EF050455; L: EF050454) from Crocidura theresea, Ash River virus (ARRV MSB73418, S: EF650086; L: EF619961) from Sorex cinereus, Yakeshi virus (YKSV Si-210, S: JX465423; M: JX465403; L: JX465389) from Sorex isodon, Kenkeme virus (KKMV MSB148794, S: GQ306148; M: GQ306149; L: GQ306150 and KKMV Fuyuan Sr326, S: NC_034559; M: KJ857337; L: KJ857320) from Sorex roboratus, and Boginia virus (BOGV 3486, L: KM394262) from Neomys fodiens. Also shown are representative rodent-borne hantaviruses (black lettering), including Sin Nombre orthohantavirus (SNV NMH10, S: NC_005216; M: NC_005215; L: NC_005217), Andes orthohantavirus (ANDV Chile9717869, S: AF291702; M: AF291703; L: AF291704), Prospect Hill orthohantavirus (PHV PH-1, S: Z49098; M: X55129; L: EF646763), Tula orthohantavirus (TULV M5302v, S: NC_005227; M: NC_005228; L: NC_005226), Puumala orthohantavirus (PUUV Sotkamo, S: NC_005224; M: NC_005223; L: NC_005225), Sangassou orthohantavirus (SANGV SA14, S: JQ082300; M: JQ082301; L: JQ082302), Soochong orthohantavirus (SOOV SOO-1, S: AY675349; M: AY675353; L: DQ056292), Dobrava/Belgrade orthohantavirus (DOBV/BGDV Greece, S: NC_005233; M: NC_005234; L: NC_005235), Hantaan orthohantavirus (HTNV 76-118, S: NC_005218; M: NC_005219; L: NC_005222), and Seoul orthohantavirus (SEOV 80-39, S: NC_005236; M: NC_005237; L: NC_005238), and Tigray virus (TIGV ET2121, S: KU934010; M: KU934009; L: KU934008) from Stenocephalemys albipes. Bat-borne hantaviruses (blue lettering) include Brno loanvirus (BRNV 7/2012/CZE, S: KX845678; M: KX845679; L: KX845680) from Nyctalus noctula, Láibīn mobatvirus (LAIV BT20, S: KM102247; M: KM102248; L: KM102249) from Taphozous melanopogon, Xuân Sơn mobatvirus (XSV VN1982B4, S: KC688335; L: JX912953) from Hipposideros pomona, Quezon mobatvirus (QZNV MT1720/1657, S: KU950713; M: KU950714; L: KU950715) from Rousettus amplexicaudatus, Mouyassué virus (MOYV KB576, L: JQ28771) from Neoromicia nanus, Makokou virus (MAKV GB303, L: KT316176) from Hipposideros ruber, Huángpí virus (HUPV Pa-1, S: JX473273, and L: JX465369) from Pipistrellus abramus, Lóngquán loanvirus (LQUV Ra-25, S: JX465415; M: JX465397; and L: JX465381) from Rhinolophus sinicus, Đakrông mobatvirus (DKGV VN2913B72, S: MG663536; M: MG663535; L: MG663534) from Aselliscus stoliczkanus, respectively. The numbers at each node are posterior node probabilities (>0.7), based on 150,000 trees: two replicate Markov Chain Monte Carlo runs consisting of six chains of 10 million generations each sampled every 100 generations with a burn-in of 25,000 (25%). The scale bar indicates the nucleotide substitutions per site.

Figure 3

Bayesian phylogenetic tree based on 1140 nucleotides of the cytochrome b mtDNA of shrews and moles (order Eulipotyphla, families Talpidae and Soricidae), rodents (order Rodentia, families Muridae and Cricetidae), and bats (order Chiroptera, suborders Yinpterochiroptera and Yangochiroptera). The tree was rooted using Elephantulus (order Macroscelidea, GenBank Nos. DQ901019, DQ901206, and DQ901201) as the outgroup. FN640579 is from a Siberian mole captured in Teletskoye. Talpa altaica from this study are shown in bolded green lettering. Other mole species harboring hantaviruses are shown in unbolded green lettering. The number at each node indicates posterior probability values (>0.7), based on 15,000 trees: two replicate Markov chain Monte Carlo runs, consisting of six chains of one million generations each sampled every 100 generations with a burn-in of 2500 (25%). The scale bar indicates the number of nucleotide substitutions per site. GenBank accession numbers are shown for taxa.