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, 27 (24), 5263-5278

Virus-virus Interactions and Host Ecology Are Associated With RNA Virome Structure in Wild Birds

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Virus-virus Interactions and Host Ecology Are Associated With RNA Virome Structure in Wild Birds

Michelle Wille et al. Mol Ecol.

Abstract

Little is known about the factors that shape the ecology of RNA viruses in nature. Wild birds are an important case in point, as other than influenza A virus, avian samples are rarely tested for viruses, especially in the absence of overt disease. Using bulk RNA-sequencing ("meta-transcriptomics"), we revealed the viral diversity present in Australian wild birds through the lens of the ecological factors that may determine virome structure and abundance. A meta-transcriptomic analysis of four Anseriformes (waterfowl) and Charadriiformes (shorebird) species sampled in temperate and arid Australia revealed the presence of 27 RNA virus genomes, 18 of which represent newly described species. The viruses identified included a previously described gammacoronavirus and influenza A viruses. Additionally, we identified novel virus species from the families Astroviridae, Caliciviridae, Reoviridae, Rhabdoviridae, Picobirnaviridae and Picornaviridae. We noted differences in virome structure that reflected underlying differences in location and influenza A infection status. Red-necked Avocets (Recurvirostra novaehollandiae) from Australia's arid interior possessed the greatest viral diversity and abundance, markedly higher than individuals sampled in temperate Australia. In Ruddy Turnstones (Arenaria interpres) and dabbling ducks (Anas spp.), viral abundance and diversity were higher and more similar in hosts that were positive for influenza A infection compared to those that were negative for this virus, despite samples being collected on the same day and from the same location. This study highlights the extent and diversity of RNA viruses in wild birds and lays the foundation for understanding the factors that determine virome structure in wild populations.

Keywords: ecology; host-pathogen interactions; influenza A virus; virome; virus evolution; wild birds.

Figures

Fig 1.
Fig 1.. Abundance of viruses in each library.
(A) Abundance of all exogenous viruses including those from avian, invertebrate, lower vertebrate, plant, fungi or bacterial hosts. (B) Abundance of all viruses that are associated with birds. (C) Abundance of retroviruses or retrovirus-like elements that have avian or mammalian signature. (D). Host reference gene RPS13.
Fig 2.
Fig 2.
Phylogenies of double-stranded RNA viruses. These trees show (a) segment 2 (RdRp) of picobirnaviruses, and (b) the VP1 segment (RdRp) of the rotaviruses described in this study. All phylogenetic trees were midpoint rooted for clarity only. The scale bar indicates the number of amino acid substitutions per site. Bootstrap values >70% are shown for key nodes. Viruses described in this study are marked with a filled circle.
Fig 3.
Fig 3.
Partial RpRp phylogeny of members of the genus Avastrovirus. The tree is rooted between the avian and mammalian astroviruses. The scale bar indicates the number of nucleotide substitutions per site. Bootstrap values >70% are shown for key nodes. Viruses described in this study are marked with a filled circle. The phylogeny of the full length polyprotein is presented in Fig S6.
Fig 4.
Fig 4.
Phylogenetic tree of the polyprotein, containing the RdRp, of members of the Caliciviridae. The most divergent calicivirus, Atlantic Salmon calicivirus, was used as an outgroup to root the tree. The scale bar indicates the number of amino acid substitutions per site. Bootstrap values >70% are shown for key nodes. Viruses described in this study are marked with a filled circle.
Fig 5.
Fig 5.
Phylogeny of the L gene (RdRp) of members of the Rhabdoviridae. Almendraviruses were set as the outgroup and representative viruses for each genus (as per (Walker et al. 2015)) were also included in the analysis. The scale bar indicates the number of amino acid substitutions per site. Bootstrap values >70% are shown for key nodes. Viruses described in this study are marked with a filled circle.
Fig 6.
Fig 6.
Phylogeny of the polyprotein, containing the RdRp, of the Picornaviridae. Reference viruses are those from (Boros et al. 2016) and the tree was midpoint rooted for clarity only. The scale bar indicates the number of amino acid substitutions per site. Bootstrap values >70% are shown for key nodes. Viruses described in this study are marked with a filled circle. The tree is mid-point rooted for clarity only.
Fig 7.
Fig 7.
Composition of avian viromes. (a) Bipartite network illustrating species for which complete viral genomes found in each library. Each library is represented as a central node, with a pictogram of the avian species, surrounded by each viral species. Where no complete viral genomes were revealed, the pictogram is shown with no viruses. Where two libraries share a virus species the networks between the two libraries are linked, and the edges are thicker for aesthetic purposes. Placement of libraries are arranged by influenza A status on the y-axis, and location on the x-axis. Virus colour corresponds to virus taxonomy. A list of viruses from each library is presented in Table S1, and phylogenetic trees for each virus family and species can be found in (Fig 2–6, Figs S3-S8). (b) Non-metric multidimensional scaling (NMDS) plot (applying the Bray Curtis dissimilarity matrix) for viral abundance and virus family diversity. Colour, shape and fill correspond to host species, influenza A infection status and location, respectively. For increased clarity, influenza A positive libraries are indicated. Additional NMDS plots where data are analysed with and without IAV reads at both the viral genus and family level are found in Figs S12-S13.
Fig 8.
Fig 8.
Influenza A status and location are associated with differences in viral abundance and diversity. A,C,E correspond to the influenza A virus infection status, while B, D, F correspond to location. (A, B) Avian viral abundance in libraries in grey, and in (A) abundance of IAV is indicated in black. (C, D) Abundance of host reference gene RSP13. (E, F) Heatmap illustrating viral diversity, at the genus level in each library, with colour corresponding to viral abundance. Blue and purple correspond to viruses with high abundance and pink correspond to viruses with low abundance. Asterisks indicate cases in which at least one complete viral genome was obtained.

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