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. 2013 Aug 20;8(8):e71595.
doi: 10.1371/journal.pone.0071595. eCollection 2013.

Metagenomic analysis of the ferret fecal viral flora

Saskia L Smits  1 , V Stalin Raj, Minoushka D Oduber, Claudia M E Schapendonk, Rogier Bodewes, Lisette Provacia, Koert J Stittelaar, Albert D M E Osterhaus, Bart L Haagmans
Affiliations

Metagenomic analysis of the ferret fecal viral flora

Saskia L Smits et al. PLoS One. .

Abstract

Ferrets are widely used as a small animal model for a number of viral infections, including influenza A virus and SARS coronavirus. To further analyze the microbiological status of ferrets, their fecal viral flora was studied using a metagenomics approach. Novel viruses from the families Picorna-, Papilloma-, and Anelloviridae as well as known viruses from the families Astro-, Corona-, Parvo-, and Hepeviridae were identified in different ferret cohorts. Ferret kobu- and hepatitis E virus were mainly present in human household ferrets, whereas coronaviruses were found both in household as well as farm ferrets. Our studies illuminate the viral diversity found in ferrets and provide tools to prescreen for newly identified viruses that potentially could influence disease outcome of experimental virus infections in ferrets.

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Conflict of interest statement

Competing Interests: The authors have the following interests. Dr. A.D.M.E. Osterhaus and Dr. S.L. Smits are part time chief scientific officer and senior scientist respectively of Viroclinics Biosciences B.V. Koert J. Stittelaar is employed by Viroclinics Biosciences B.V. There are no patents, products in development or marketed products to declare. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials, as detailed online in the guide for authors.

Figures

Figure 1
Figure 1. Prevalence of ferret viruses.
Percentage coronavirus (A), hepatitis E virus (B) and kobuvirus (C) positive farm versus household ferrets by real time PCR assay. Significant differences (unpaired t-test P<0.05) are indicated by an asterisk.
Figure 2
Figure 2. Genome organization of ferret kobuvirus and amino acid sequence divergence from other aichiviruses.
(A) Predicted genome organization of ferret kobuvirus showing amino acid positions of predicted cleavage sites in the polyprotein (numbering based on the ferret kobuvirus polyprotein sequence). Sites were predicted by NetPicoRNA analysis and by alignment with known cleavage sites in aichiviruses. (B) Mean similarity of bovine kobuvirus (AB084788) to ferret kobuvirus (red), porcine kobuvirus (GU292559, green), and human aichivirus (FJ890523; blue) polyprotein-coding nucleotide sequences scaled to the genome diagram in A. (C–E) Phylogenetic trees of the amino acid sequences of ferret kobuvirus (MpKoV32, 38, and 39) with other aichiviruses in the P1 (C), P2 (D), and P3 (E) gene regions were generated using MEGA5, with the neighbor-joining method with p-distance and 1,000 bootstrap replicates. Significant bootstrap values are shown.
Figure 3
Figure 3. Genome organization and phylogenetic analysis of ferret parechovirus.
(A) Predicted genome organization of ferret parechovirus showing amino acid positions of predicted cleavage sites in the polyprotein (numbering based on the ferret parechovirus polyprotein sequence). Sites were predicted by NetPicoRNA analysis and by alignment with other parechoviruses. (B) A phylogenetic tree of the polyprotein sequence of ferret parechovirus (MpPeV1) and representative human (HPeV1-8) and bank vole parechoviruses (Ljungan virus) was generated using MEGA5, with the neighbor-joining method with p-distance and 1,000 bootstrap replicates and human rhinovirus A 86 as an outgroup (HRV-A 86). Significant bootstrap values are shown. Genbank accession numbers are shown in Table S1.
Figure 4
Figure 4. Genome organization of ferret papillomavirus and nucleotide sequence divergence from other papillomaviruses.
(A) Predicted genome organization of ferret papillomavirus with early (E) and late (L) genes indicated. (B) A phylogenetic tree of the complete ferret papillomavirus (MpPV1) genome and representative human and animal papillomaviruses was generated using MEGA5, with the maximum-likelihood method with Kimura-2 parameter and 1,000 bootstrap replicates. Significant bootstrap values are shown. (C) A phylogenetic tree of the L1 genome region of ferret papillomavirus (MpPV1) and representative human and animal papillomaviruses was generated using MEGA5, with the maximum-likelihood method with Kimura-2 parameter and 1,000 bootstrap replicates. Significant bootstrap values are shown. Genbank accession numbers are shown in Table S1.
Figure 5
Figure 5. Phylogenetic analysis of ferret anellovirus.
A phylogenetic tree of the partial ORF1 nucleotide sequence of ferret torque teno virus (MpfTTV1) and the corresponding region of representative human and animal anelloviruses was generated using MEGA5, with the neighbor-joining method with p-distance and 1,000 bootstrap replicates. Significant bootstrap values are shown. Genbank accession numbers are shown in Table S1.
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Grants and funding

The research leading to these results has received funding from the European Community's Seventh Framework Programme (FP7/2007–2013) under the project “European Management Platform for Emerging and Re-emerging Infectious disease Entities” (EMPERIE) EC grant agreement number 223498 and the Virgo consortium. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.