Genetically distinct hantaviruses in two bat species in Panamá

Abstract

Recent discoveries of hantaviruses in bats in Europe, Asia, and Africa have prompted expanded explorations of their host diversity and geographic distribution. In screening lung tissue of 218 bats from Panamá, representing 19 genera and five families, we detected hantavirus RNA in two of three greater sac-winged bats (Emballonuridae: Saccopteryx bilineata) and in four of 29 Seba's short-tailed bats (Phyllostomidae: Carollia perspicillata). Phylogenetic analyses of the small, medium, and large genomic segments revealed a newfound hantavirus in S. bilineata, tentatively designated Filo del Tallo virus, and the recently reported Buritiense virus in C. perspicillata. Both share common ancestry with bat-associated hantaviruses in Asia and Africa. These results indicate that bats serve as hosts of hantaviruses in the Americas. Given opportunities for close contact between humans and bats, studies on the genetic diversity, pathogenicity, and circulation dynamics of hantaviruses are urgently needed.

Keywords: Microbiology; Virology; Zoology.

Graphical abstract

Figure 1

Host geographic distributions and sampling (A and B) Map of Central and South America showing the geographic range of the Seba’s short-tailed bat (Carollia perspicillata) (blue, A) and the greater sac-winged bat (Saccopteryx bilineata) (yellow, B). The scale bars represent 2,000 km (A and B). (C) Capture sites are shown in Metetí (S1: Centro Regional Universitario Darién, S2: Filo del Tallo) and Yaviza (S3: Instituto Forestal y Agropecuario del Darién) in the Darién Province of Panamá. The scale bar represent 200 km (C). (D–F) Distribution data for C. perspicillata and S. bilineata were downloaded from the International Union for the Conservation of Nature (IUCN) Red List of Threatened Species (downloaded on Mar 25, 2024). Composition of host families—Emballonuridae (navy), Mormoopidae (orange), Noctilionidae (dark green), Phyllostomidae (light blue), and Vespertilionidae (purple)—at each capture site are shown for Centro Regional Universitario Darién (D), Filo del Tallo (E), and Instituto Forestal y Agropecuario del Darien (F).

Figure 2

Topological and structural organization of the glycoproteins Gn and Gc of a representative bat-borne hantavirus, Đakrông mobatvirus (DKGV) (A) The topological structure of DKGV glycoproteins, showing the signal peptide (red), N-glycosylation motif (dark green), YXXL/I immunoreceptor tyrosine-based activation motif (ITAM) (bright yellow green), Zinc finger motifs (ZF) (yellow and orange), nucleocapsid protein binding site (NBS) (blue), cytoplasmic tail (gray), WAASA predicted cleavage site (light blue), and predicted fusion loop (fuchsia). Numbers 1–3 indicate transmembrane regions. (B) Predicted transmembrane structure of Andes orthohantavirus (ANDV), DKGV, Filo del Tallo virus (FDTV8753) strain 8753, and Buritiense virus (BRIV8832) strain 8832. (C and D) Transmembrane (C) and ITAM motifs (I1S and I2S) (D) were detected in alignment of amino acid sequences of ANDV, Nova mobatvirus (NVAV), Xuân Sơn mobatvirus (XSV), Láibīn mobatvirus (LAIV), Sarawak virus (SRWV), Brno loanvirus (BRNV), Lóngquán loanvirus (LQUV), Quezon mobatvirus (QZNV), Robina virus (RBNV), FDTV, BRIV, Huángpí virus (HUPV), Mouyassué virus (MOYV), and Hǎinán oriental leaf-toed gecko hantavirus (HOLGV). The motifs (YXXL/I) were confirmed in ANDV, DKGV, and LAIV (red star). FDTV8753, FDTV8767, and BRIV8832, reported in this study, are shown (light blue star). (E) Amino acid sequences predicted for NBS and ZF. B1 and B2 and ZF1 and ZF2 are indicated as NBS and Zinc finger motifs, respectively. Conserved amino acids are shown with asterisks.

Figure 3

Phylogenetic analysis of hantaviruses (A and B) Host species classification, distribution map, and phylogenetic analyses for selected hantaviruses indicated in list (A) and geoscheme map (B). (C–H) Phylogenetic trees based on nucleotide sequences of the (C) small-, (D) medium-, and (E) large-genomic segments of the hantavirus genome and amino acid sequences of the (F) nucleocapsid protein (NP), (G) envelope glycoprotein (GP), and (H) RNA-dependent RNA polymerase (RdRP), respectively, generated by the Bayesian Markov chain Monte Carlo estimation method. The numbers at each node are SH-aLRT support (>70%)/ultrafast bootstrap support (>70%)|Bayesian posterior probabilities (>0.7). Scale bars indicate the number of nucleotide substitutions per site.

Figure 4

Co-phylogenetic analysis (A and B) Phylogenetic and cophylogenetic analysis, based on (A) 1,140 bp of the cytb mitochondrial gene from small mammals within the orders Eulipotyphla (families Soricidae and Talpidae), Rodentia (families Muridae and Cricetidae), and Chiroptera, suborders Yinpterochiroptera (families Pteropodidae, Hipposideridae, Rhinolophidae, and Megadermatidae) and Yangochiroptera (families Nycteridae, Molossidae, Vespertilionidae, Emballonuridae, and Phyllostomidae), and (B) amino acid tangle of RNA-dependent RNA polymerase (RdRP). The tree was rooted using Hemidactylus bowringii (order Squamata) as the outgroup. Node labels indicate posterior probabilities (A). FDTV and BRIV are shown in turquoise blue and red, respectively. FDTV and BRIV strains reported in this study are shown in bold text. The color definition was the same pattern as in Figure 3A.