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. 2019 Aug 21;11(9):768.
doi: 10.3390/v11090768.

Discovery and Characterization of Novel RNA Viruses in Aquatic North American Wild Birds

Marta Canuti  1 , Ashley N K Kroyer  2 , Davor Ojkic  3 , Hugh G Whitney  2 , Gregory J Robertson  4 , Andrew S Lang  5
Affiliations

Discovery and Characterization of Novel RNA Viruses in Aquatic North American Wild Birds

Marta Canuti et al. Viruses. .

Abstract

Wild birds are recognized viral reservoirs but our understanding about avian viral diversity is limited. We describe here three novel RNA viruses that we identified in oropharyngeal/cloacal swabs collected from wild birds. The complete genome of a novel gull metapneumovirus (GuMPV B29) was determined. Phylogenetic analyses indicated that this virus could represent a novel avian metapneumovirus (AMPV) sub-group, intermediate between AMPV-C and the subgroup of the other AMPVs. This virus was detected in an American herring (1/24, 4.2%) and great black-backed (4/26, 15.4%) gulls. A novel gull coronavirus (GuCoV B29) was detected in great black-backed (3/26, 11.5%) and American herring (2/24, 8.3%) gulls. Phylogenetic analyses of GuCoV B29 suggested that this virus could represent a novel species within the genus Gammacoronavirus, close to other recently identified potential novel avian coronaviral species. One GuMPV-GuCoV co-infection was detected. A novel duck calicivirus (DuCV-2 B6) was identified in mallards (2/5, 40%) and American black ducks (7/26, 26.9%). This virus, of which we identified two different types, was fully sequenced and was genetically closest to other caliciviruses identified in Anatidae, but more distant to other caliciviruses from birds in the genus Anas. These discoveries increase our knowledge about avian virus diversity and host distributions.

Keywords: avian viruses; calicivirus; coronavirus; metapneumovirus; novel viruses; viral epidemiology; virus discovery.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Molecular characteristics of GuMPV B29. The genome organization of the novel virus is depicted at the top. Identified open reading frames (ORFs) are illustrated by colored rectangles: Nonstructural proteins are in green (N: nucleoprotein; P: phosphoprotein, L: polymerase), envelope glycoproteins are in yellow (F: fusion protein; SH: small hydrophobic protein; G: glycoprotein), and the matrix protein (M) is in pink. The scale bar on top represents genomic position in Kb. The phylogenetic placement of GuMPV B29 within the genus Metapneumovirus based on the complete amino acid sequence of the L protein is shown at the bottom. The two species Human metapneumovirus (AMPV) and Avian metapneumovirus (AMPV) are indicated on the right, and the murine pneumovirus (MPV) was used as an outgroup. Accession numbers are indicated in parentheses. Officially assigned viral sub-groups are indicated by letters (A1-2, B1-2 for HMPV, A–D for AMPV), while recently identified viruses that lack official taxonomic designations are indicated by circles with the virus identified in this study indicated by the filled green circle. The tree was built with the maximum likelihood method [47] using MEGA 7 [43] based on the Le Gascuel model [49], identified as the best-fitting model by the model test in MEGA. A discrete Gamma distribution was used to model evolutionary rate differences among sites, branch lengths are proportional to genetic distances as indicated by the scale bar, and the outcome of the bootstrap analysis [48] is shown next to the nodes.
Figure 2
Figure 2
Molecular characteristics of GuCoV B29. The organization of the partial 1a polyprotein of the novel virus is depicted at the top. Identified mature peptides (non-structural proteins, nsp1/2–7) are illustrated by green rectangles. The pink rectangle indicates the area in nsp3 where the tandem repeat (TR) was identified, while the yellow rectangle shows the location of the conserved ADP-ribose 1-“phosphatase (ADRP) replicase domain within nsp3. The scale bar on top represents the amino acid position within the polyprotein. The phylogenetic placement of GuCoV B29 within the genus Gammacoronavirus based on the concatenated alignments of the ADRP and 3C-like proteinase (3CLpro) (corresponding to nsp5) is shown at the bottom. The two species Igacovirus and Cegacovirus are indicated on the right. Accession numbers of sequences used (SW1: Beluga whale coronavirus; BdCoV: Bottlenose dolphin coronavirus; IBV: Infectious bronchitis virus; TCoV: Turkey coronavirus; GfCoV: Guinea fowl coronavirus; DdCoV: Dominant-duck coronavirus; GuCoV: Gull coronavirus; CGCoV: Canada goose coronavirus) are indicated in parentheses. Recently identified viruses that lack official taxonomic designations are indicated by circles with the virus identified in this study indicated by the filled green circle. The tree was built with the maximum likelihood method [47] using MEGA 7 [43] based on the Le Gascuel model [50], identified as the best-fitting model by the model test in MEGA. A discrete Gamma distribution was used to model evolutionary rate differences among sites, branch lengths are proportional to genetic distances as indicated by the scale bar, and the outcome of the bootstrap analysis [48] is shown next to the nodes.
Figure 3
Figure 3
Molecular characteristics of DuCV-2 B6. The genome organization of the novel virus is depicted at the top. The two identified ORFs are illustrated by green rectangles, while nonstructural and structural protein regions are indicated in yellow and pink, respectively. Enzymatic domains typical of caliciviruses are indicated (H: helicase/NTPase; P: 3C-like cysteine protease; RdRp: RNA-dependent RNA polymerase) and the scale bar above indicates genomic position in Kb. The phylogenetic placement of DuCVs-2 B6 and B76 within the genus Nacovirus based on the predicted amino acid sequence of the major capsid protein (VP1) is shown at the bottom. Hosts of viruses used for phylogenetic reconstruction are indicated within the strain designation (PeDu: Pink-eared duck; Du: Duck; Go: Goose; Av: Avocet; Cr: Crane; Tu: Turkey; Ch: Chicken; Gt: Grey teal; Rt: Ruddy turnstone; Sd: Shelduck; Hu: Human; Po: Porcine), while accession numbers of sequences are indicated in parentheses. Viral genera are depicted on the right and the two mammalian caliciviruses of the genus Sapovirus were used as an outgroup. Recently identified viruses that lack official taxonomic designation are indicated by circles and the viruses identified in this study are indicated by filled green circles. The tree was built with the maximum likelihood method [47] using MEGA 7 [43] based on the Le Gascuel model [50], identified as the best-fitting model by the model test in MEGA. A discrete Gamma distribution was used to model evolutionary rate differences among sites, branch lengths are proportional to genetic distances as indicated by the scale bar, and the outcome of the bootstrap analysis [48] is shown next to the nodes.
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