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Complete genome sequence of a novel sea otterpox virus

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Abstract

Members of the Poxviridae family are large, double-stranded DNA viruses that replicate in the cytoplasm of their host cells. The subfamily Chordopoxvirinae contains viruses that infect a wide range of vertebrates including marine mammals within the Balaenidae, Delphinidae, Mustelidae, Odobenidae, Otariidae, Phocidae, and Phocoenidae families. Recently, a novel poxvirus was found in a northern sea otter pup (Enhydra lutris kenyoni) that stranded in Alaska in 2009. The phylogenetic relationships of marine mammal poxviruses are not well established because of the lack of complete genome sequences. The current study sequenced the entire sea otterpox virus Enhydra lutris kenyoni (SOPV-ELK) genome using an Illumina MiSeq sequencer. The SOPV-ELK genome is the smallest poxvirus genome known at 127,879 bp, is 68.7% A+T content, is predicted to encode 132 proteins, and has 2546 bp inverted terminal repeats at each end. Genetic and phylogenetic analyses based on the concatenated amino acid sequences of 7 chorodopoxvirus core genes revealed the SOPV-ELK is 52.5–74.1% divergent from other known chordopoxviruses and is most similar to pteropoxvirus from Australia (PTPV-Aus). SOPV-ELK represents a new chordopoxvirus species and may belong to a novel genus. SOPV-ELK encodes eight unique genes. While the function of six predicted genes remains unknown, two genes appear to function as novel immune-modulators. SOPV-ELK-003 appears to encode a novel interleukin-18 binding protein (IL-18 BP), based on limited sequence and structural similarity to other poxviral IL-18 BPs. SOPV-ELK-035 appears to encode a novel tumor necrosis factor receptor-like (TNFR) protein that may be associated with the depression of the host’s antiviral response. Additionally, SOPV-ELK-036 encodes a tumor necrosis factor-like apoptosis-inducing ligand (TRAIL) protein that has previously only been found in PTPV-Aus. The SOPV-ELK genome is the first mustelid poxvirus and only the second poxvirus from a marine mammal to be fully sequenced. Sequencing of the SOPV-ELK genome is an important step in unraveling the position of marine mammal poxviruses within the larger Poxviridae phylogenetic tree and provides the necessary sequence to develop molecular tools for future diagnostics and epidemiological studies.

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Acknowledgements

We would like to thank the University of Florida Graduate Student Fellowship for providing financial support.

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Authors and Affiliations

  1. Department of Infectious Diseases and Immunology, College of Veterinary Medicine, University of Florida, Gainesville, FL, 32610, USA

    Jessica M. Jacob, Kuttichantran Subramaniam & Thomas B. Waltzek

  2. Biochemistry and Microbiology Department, University of Victoria, Victoria, BC, V8W 2Y2, Canada

    Shin-Lin Tu & Chris Upton

  3. Department of Fisheries and Oceans Canada, Central and Arctic Region, Winnipeg, MB, R3T 2N6, Canada

    Ole Nielsen

  4. Alaska SeaLife Center, Seward, AK, 99664, USA

    Pamela A. Tuomi

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  1. Jessica M. Jacob
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  2. Kuttichantran Subramaniam
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Contributions

PAT provided the northern sea otter lesion sample. ON isolated the virus using standard cell culture techniques. JMJ, KS, CU, SLT, TBW completed genome assembly and annotation. JMJ, TBW, KS, SLT, CU wrote the manuscript.

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Correspondence to Thomas B. Waltzek.

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The authors declare that they have no conflict of interest.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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Edited by William Dundon.

Electronic supplementary material

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11262_2018_1594_MOESM1_ESM.pdf

Supplementary material 1—Fig. S1 Sea otterpox virus annotated genome. The SOPV-ELK genome is 127,879 bp, 68.7% A+T, encodes 132 predicted proteins, and has 2546 bp ITRs. The 4 genes contained within the ITRs are represented by the red arrows. The 49 Poxviridae core genes are represented by the green arrows. The 31 Chordopoxvirinae core genes are represented by the purple arrows. The 8 genes that are unique to the SOPV-ELK are represented by the blue arrows. The 9 genes that are only present in both the SOPV-ELK and PTPV-Aus are represented by the grey arrows. The remaining 31 non-core poxvirus genes are represented by the yellow arrows (PDF 166 KB)

11262_2018_1594_MOESM2_ESM.pdf

Supplementary material 2—Fig. S2 Amino acid percent similarity for 46 poxviruses. Sequence identity matrix showing the amino acid percent similarity of the SOPV-ELK to 45 poxviruses based on the concatenated amino acid (aa) sequences of 7 conserved genes: RNA polymerase subunit RPO147, RNA polymerase subunit RPO132, RNA polymerase-associated RAP94, mRNA capping enzyme large subunit, virion major core protein P4a, early transcription factor VETFL, and NTPase. See Table 1 for virus abbreviations (PDF 429 KB)

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Jacob, J.M., Subramaniam, K., Tu, SL. et al. Complete genome sequence of a novel sea otterpox virus. Virus Genes 54, 756–767 (2018). https://doi.org/10.1007/s11262-018-1594-8

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