The ecology, genetic diversity, and phylogeny of Huaiyangshan virus in China

Abstract

Surveys were carried out to better understand the tick vector ecology and genetic diversity of Huaiyangshan virus (HYSV) in both regions of endemicity and regions of nonendemicity. Haemaphysalis longicornis ticks were dominant in regions of endemicity, while Rhipicephalus microplus is more abundant in regions of nonendemicity. HYSV RNA was found in human and both tick species, with greater prevalence in H. longicornis and lesser prevalence in R. microplus. Phylogenetic analyses indicate that HYSV is a novel species of the genus Phlebovirus.

Fig 1

Map showing the locations of tick collection sites in regions of endemicity (orange) and regions of nonendemicity of hemorrhagic fever caused by Huaiyangshan virus (HYSV) in Henan and Hubei provinces. The red circles represent the cases diagnosed in 2009 and 2010. The blue triangles represent the sites in which ticks were collected, and the green five-pointed stars represent the sites in which HYSV RNA-positive ticks were collected.

Fig 2

Phylogenetic relationship of Huaiyangshan viruses (HYSV) from humans and ticks. The trees were constructed based on the partial L segment sequences (A) and the partial S segment sequences (B) by using the neighbor-joining (NJ) method. Seoul virus (SEOV) was used as the outgroup. Numbers (>50%) at the branch nodes indicate bootstrap values obtained by NJ analysis. Red and blue colors highlight HYSV strains identified from humans and ticks obtained in this study, respectively. The GenBank accession numbers of the L and S segment sequences of other viruses are listed in parentheses as follows: Massilia virus (MASV; EU725771 and EU725773, respectively), Toscana virus (TOSV; NC_006319 and NC_006318), Rift Valley fever virus (RVFV; DQ375406 and DQ380149), sandfly fever Sicilian virus (SFSV; GQ847513 and GQ847511), and Uukuniemi virus (UUKV; D10759 and M33551). HYSV (or SFTSV) strains isolated by Yu et al. (14) include Shandong 4 (HM802202 and HM802204), Shandong 24 (HM802205 and HM802200), Liaoning 2 (HQ141607 and HQ141609), Liaoning 3 (HQ141610 and HQ141612), Henan 6 (HQ141595 and HQ141597), Henan 13 (HQ141598 and HQ141600), Anhui 12 (HQ116417 and HQ141591), Anhui 15 (HQ141592 and HQ141594), Hubei 29 (HM745930 and HM745932), Jiangsu 3 (HQ141601 and HQ141603), Jiangsu 4 (HQ141604 and HQ141606), Jiangsu 6 (HQ830169 and HQ830171), Jiangsu 24 (HQ830163 and HQ830165), and Jiangsu 26 (HQ830166 and HQ830168). HYSV strains recovered from patients in our previous study are 2009-11 (HQ171186 and HQ171191), 2010-2 (HQ171190 and HQ171195), 2010-4 (HQ171187 and HQ171192), 2010-13 (HQ419226; no S sequence was used), 2010-15 (HQ171189 and HQ171194), 2010-16 (HQ171188 and HQ171193), 2010-17 (HQ179737; no L sequence was used), 2010-18 (HQ179708 and HQ179940), and 2010-19 (HQ179744; no L sequence was used). The GenBank accession numbers of the L segment sequences of HYSV from ticks from our previous study are HQ419223 to HQ419225. These sequences are described in more detail in Table S1 in the supplemental material.

Fig 2

Phylogenetic relationship of Huaiyangshan viruses (HYSV) from humans and ticks. The trees were constructed based on the partial L segment sequences (A) and the partial S segment sequences (B) by using the neighbor-joining (NJ) method. Seoul virus (SEOV) was used as the outgroup. Numbers (>50%) at the branch nodes indicate bootstrap values obtained by NJ analysis. Red and blue colors highlight HYSV strains identified from humans and ticks obtained in this study, respectively. The GenBank accession numbers of the L and S segment sequences of other viruses are listed in parentheses as follows: Massilia virus (MASV; EU725771 and EU725773, respectively), Toscana virus (TOSV; NC_006319 and NC_006318), Rift Valley fever virus (RVFV; DQ375406 and DQ380149), sandfly fever Sicilian virus (SFSV; GQ847513 and GQ847511), and Uukuniemi virus (UUKV; D10759 and M33551). HYSV (or SFTSV) strains isolated by Yu et al. (14) include Shandong 4 (HM802202 and HM802204), Shandong 24 (HM802205 and HM802200), Liaoning 2 (HQ141607 and HQ141609), Liaoning 3 (HQ141610 and HQ141612), Henan 6 (HQ141595 and HQ141597), Henan 13 (HQ141598 and HQ141600), Anhui 12 (HQ116417 and HQ141591), Anhui 15 (HQ141592 and HQ141594), Hubei 29 (HM745930 and HM745932), Jiangsu 3 (HQ141601 and HQ141603), Jiangsu 4 (HQ141604 and HQ141606), Jiangsu 6 (HQ830169 and HQ830171), Jiangsu 24 (HQ830163 and HQ830165), and Jiangsu 26 (HQ830166 and HQ830168). HYSV strains recovered from patients in our previous study are 2009-11 (HQ171186 and HQ171191), 2010-2 (HQ171190 and HQ171195), 2010-4 (HQ171187 and HQ171192), 2010-13 (HQ419226; no S sequence was used), 2010-15 (HQ171189 and HQ171194), 2010-16 (HQ171188 and HQ171193), 2010-17 (HQ179737; no L sequence was used), 2010-18 (HQ179708 and HQ179940), and 2010-19 (HQ179744; no L sequence was used). The GenBank accession numbers of the L segment sequences of HYSV from ticks from our previous study are HQ419223 to HQ419225. These sequences are described in more detail in Table S1 in the supplemental material.