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A novel polyomavirus from the nasal cavity of a giant panda (Ailuropoda melanoleuca)

  • 1, 2,
  • 3,
  • 2,
  • 4,
  • 1,
  • 1,
  • 1,
  • 1,
  • 5,
  • 5,
  • 4,
  • 1Email author and
  • 2Email author
Contributed equally
Virology Journal201714:207

https://doi.org/10.1186/s12985-017-0867-5

  • Received: 12 February 2017
  • Accepted: 11 October 2017
  • Published:

Abstract

Background

Polyomaviruses infect a wide variety of mammalian and avian hosts with a broad spectrum of outcomes including asymptomatic infection, acute systemic disease, and tumor induction.

Methods

Viral metagenomics and general PCR methods were used to detected viral nucleic acid in the samples from a diseased and healthy giant pandas.

Results

A novel polyomavirus, the giant panda polyomavirus 1 (GPPyV1) from the nasal cavity of a dead giant panda (Ailuropoda melanoleuca) was characterized. The GPPyV1 genome is 5144 bp in size and reveals five putative open-reading frames coding for the classic small and large T antigens in the early region, and the VP1, VP2 and VP3 capsid proteins in the late region. Phylogenetic analyses of the large T antigen of the GPPyV1 indicated GPPyV1 belonged to a putative new species within genus Deltapolyomavirus, clustering with four human polyomavirus species. The GPPyV1 VP1 and VP2 clustered with genus Alphapolyomavirus. Our epidemiologic study indicated that this novel polyomavirus was also detected in nasal swabs and fecal samples collected from captive healthy giant pandas.

Conclusion

A novel polyomavirus was detected in giant pandas and its complete genome was characterized, which may cause latency infection in giant pandas.

Keywords

  • Giant panda
  • Polyomavirus
  • Complete genome

Background

Members of the family Polyomaviridae are small viruses characterized by a non-enveloped icosahedral capsid and a circular double-stranded DNA genome of approximately 5000 bp. Early and late genes are transcribed bi-directionally, starting from a short non-coding regulatory region. Early genes encode two or three proteins, designated tumor antigens, which participate in viral genome replication and cellular transformation. The late genes encode the major and minor capsid proteins VP1, VP2, and VP3 [1]. In addition, some of the primate and human polyomaviruses encode an additional non-structural multifunctional protein, the agnoprotein [2]. The International Committee on Taxonomy of Viruses (ICTV) officially lists 73 species as polyomaviruses and divides the family into 4 genera including Alpha-, Beta-, Gamma- and Deltapolyomavirus [3].

Many mammalian polyomaviruses cause subclinical infections with life-long persistence in their immune competent hosts [4]. Only some of the polyomaviruses have been described to cause disease in immune-compromised hosts [5]. Polyomavirus-related diseases, which include nephritis [6], encephalitis [7], Merkel cell carcinoma [8], skin dysplasia [9, 10], and pneumonitis [11, 12], can occur among immune-suppressed individuals, including post-transplantation and AIDS patients. Polyomaviruses are widely distributed among mammalian and avian species and besides humans they have been identified in monkeys, cattle, rabbits, raccoons, rodents, bats, elephants, badgers, and a wide variety of birds [1324].

In the present study, using viral metagenomics we detected a novel polyomavirus, the giant panda polyomavirus 1 (GPPyV1), in the nasal cavity of a giant panda (Ailuropoda melanoleuca) who died for unknown reasons after released into the wild.

Materials and methods

Samples

In July 2016, a two-year old captive giant panda was released to the wild environment of the Liziping Nature Reserve in YaAn, Sichuan Province, China. The giant panda was found dead on 27 September of the same year, having lost about 30% of its weight. Autopsy indicated that the gastrointestinal tract was complete empty and no feces were found near its body. The nasal secretion and tissues including heart, liver, spleen, lung, pancreas, muscle, testis, thyroid, and kidney tissues were collected for viral nucleic acid detection. All samples were collected by disposable materials and shipped on dry ice. The rayon ball of the nasal swab was put into the conical tube containing 1 mL PBS. The tube was then vigorously vortexed for 5 min and incubated for 30 min in 4 °C. The supernatants were then collected after centrifugation (10 min, 15,000×g). Tissue samples (~25 mg) were homogenized, frozen and thawed three times on dry ice, the supernatants were then collected after centrifugation (10 min, 15,000×g).

Viral metagenomic analysis

500 μl of each supernatant was filtered through a 0.45-μm filter (Millipore) to remove eukaryotic and bacterial cell-sized particles. The filtrates enriched in viral particles were treated with DNase and RNase to digest unprotected nucleic acid at 37 °C for 60 min [2527]. Remaining total nucleic acid was then isolated using QiaAmp Mini Viral RNA kit (Qiagen) according to manufacturer’s protocol. Four libraries were then constructed using Nextera XT DNA Sample Preparation Kit (Illumina) and sequenced using the MiSeq Illumina platform with 250 bases paired ends with dual barcoding for each library. Three libraries were constructed using tissue samples, each including three types tissues. One library consisted of the nasal swab sample. For bioinformatics analysis, paired-end reads of 250 bp generated by MiSeq were debarcoded using vendor software from Illumina. An in-house analysis pipeline running on a 32-nodes Linux cluster was used to process the data. Clonal reads were removed and low sequencing quality tails were trimmed using Phred quality score ten as the threshold. Adaptors were trimmed using the default parameters of VecScreen which is NCBI BLASTn with specialized parameters designed for adapter removal. The cleaned reads were de-novo assembled by SOAPdenovo2 version r240 using Kmer size 63 with default settings. The assembled contigs, along with singlets were aligned to an in-house viral proteome database using BLASTx with an E-value cutoff of <10−5 [28].

Genome sequencing and PCR screening

After identifying polyomavirus sequences in the nasal swab, inverse PCR was used to generate the complete genome of the novel polyomavirus. The inverse primers were designed based on a 712 bases contig: InPoFP (5′-*G* AATGGTGTGGGCCCACTATG-3′) and InPoRP (5′-*G* TTTGTCCGCCAGTGTAGCTT-3′) were used for the 1st round PCR and InPoFF (5′- GATGCAGTACCGTGGATTGC-3′) and InPoRF(5′- TTGGAGGGATCAGGACACCA-3′) for the 2nd round PCR. Here, the bases with asterisk means phosphorothioation. In order to investigate the prevalence of the novel polyomavirus in the captive giant pandas, 13 nasal swabs and 25 fecal samples were collected from healthy captive giant pandas in Chengdu Panda breeding center, and were subjected to nested PCR screening using primers, also designed based on the 712 bp partial VP1 gene sequence, including PoscrFP (5′ TGGTGTCCTGATCCCTCCAA-3′) and PoscrRP (5′- TCCAGGCAAAGGCTCAGTTC-3′) for the 1st round PCR and IPoscrFF (5′- AAGCTACACTGGCGGACAAA-3′) and PoscrRF(5′- CTGACCTTCCATTGTGGGCA-3′) for the 2nd round PCR. The original polyomavirus positive nasal swab sample was used as positive control in the PCR screening. Sanger method was used for sequencing of the inverse and regular PCR products.

Phylogenetic analysis

Phylogenetic analyses were performed based on the predicted amino acid sequence in the present study, their closest viral relatives based on the best BLASTp hits in GenBank, and representative members of related viral species or genera. Sequence alignment was performed using CLUSTAL W with the default settings. Phylogenetic trees with 500 bootstrap resamples of the alignment data sets were generated using the Maximum-likelihood (ML) method in MEGA5.0. Putative ORFs in the viral genome were predicted by combining Geneious 8.1 software and NCBI ORF finder. Putative exon and intron were predicted by Netgenes2 at http://www.cbs.dtu.dk/services/NetGene2/.

Nucleotide sequence accession numbers

The novel polyomavirus genome of GPPyV1 and sequence generated by PCR screening were deposited in GenBank under the following accession numbers: KY612371 and MF370864.

Results

DNA libraries from samples of giant pandas were generated and sequenced using the lllumina MiSeq platform. In the nasal sample 17 sequence reads generating 3 different contigs were found to have strong amino acid homology to polyomaviruses. PCR screening of all the samples from the dead wild giant panda, plus 30 other nasal swab samples and 200 fecal samples collected from healthy captive giant pandas in the the Chengdu Research Base of Giant Panda Breeding in China with a set of nested primers designed on the VP1 sequence. Results indicated that one nasal swab and two fecal samples from healthy captive giant pandas and only the nasal swab from the dead animal were positive, which suggests that polyomavirus may establish latency infection in the gastrointestinal tract and nasal cavity of giant pandas.

Sequence analysis based on the 299 bp fragments generated PCR screening, the 3 sequences from the healthy giant pandas were identical and showed only one nucleotide difference from the sequence from the died giant panda, suggesting these polyomavirus sequences may be from the same ancestor virus which was prevalent in the giant panda group. Using inverse PCR, the complete genome was then acquired and sequenced by Sanger walking from the nasal sample of the dead giant panda. The circular genome of the giant panda polyomavirus (named GPPyV1) was 5144 bases, with the overall GC content of 41.8%, which is similar to those of BK (39%), JC (40%), WU (39%) and other polyomaviruses [29]. The genome organization includes an early region coding on one strand for the small T antigen (STAg) and the large T antigen (LTAg), and a late region coding on the opposite strand for the capsid proteins VP1, VP2, and VP3, with a noncoding regulatory region between the beginning of the early region and the beginning of the late region, homologous to earlier described polyomaviruses (Fig. 1). Two copies of the consensus pentanucleotide LTAg binding site GAGGC, or the reverse complement GCCTG were present in the a noncoding regulatory region, where the sequence is GAGGCAGAAGGCCTC which might represent the possible core of the origin of replication [2]. The noncoding region between the ends of the late and early regions (Fig. 1) showed an AT-rich region. The sizes of the proteins deduced from the genome sequences of GPPyV1, their calculated molecular weights and isoelectric points are shown in Table 1.
Fig. 1
Fig. 1

Schematic of the giant panda polyomavirus 1 (GPPyV1) genome organization

Table 1

Size and position of predicted open reading frames (ORF) of GPPyV1, the predicted molecular masses (kiloDalton), and the isoelectric point (pI) of the translated proteins

ORF

Position

Length

MW (kDa)

pI

nt

aa

URR*

1–354

n/a

n/a

n/a

n/a

VP2

355–1278

924

307

33.69

4.73

VP3

571–1278

708

235

26.55

6.37

VP1

1247–2575

1329

442

48.07

6.88

NCR**

2576–2616

n/a

n/a

n/a

n/a

LTAg

2617–4548

2172

723

81.57

6.38

4905–5144

STAg

4566–5144

579

192

22.54

8.43

*Upstream regulatory region

**Noncoding region

A more detailed analysis of the amino acid sequences of GPPyV1 revealed conserved sequences in functionally important regions of the encoded proteins. The proteins encoded by the 5 GPPyV1 open-reading frames contain the typical elements that are necessary to accomplish their function in the viral life cycle of polyomaviruses. The unspliced early mRNA of GPPyV1 encodes the STAg, which is 192 aa in length, where the CXCX2C consensus sequence for protein phosphatase 2A binding is present. The initial 80 amino acids of the N-terminus of the STAg and LTAg of GPPyV1 are identical, which is a general characteristic in all polyomaviruses. The LTAg is generated by partial splicing of the early mRNA transcript. Conserved features like the J-domain, which is important for efficient DNA replication and transformation, is found in the LTAg sequence. This domain contains the highly conserved HPDKGG box and a pRB-binding motif LXCXE, which are crucial for DNA replication [9].

To determine the genetic relationship between GPPyV1 and the other related polyomaviruses. Phylogenetic analysis based on the putative LTAg amino acid sequences of polyomaviruses, including GPPyV1, the representative polyomavirus species of the four genera, and the best BLASTp searching matches of GPPyV1 in GenBank, were performed and maximum-likelihood (ML) tree was generated. Results indicated that GPPyV1 is highly divergent from these other polyomaviruses and that it fell within the clade of genus Deltapolyomavirus together with four species from human, sharing the highest amino acid sequence identity of 53% of with MW polyomavirus (GenBank no. JQ898291) (Fig. 2A). BLASTp searches in GenBank based on the amino acid sequences of VP1 and VP2 indicated GPPyV1 showed the closest relationship with polyomaviruses within genus Alphapolyomavirus which includes bat polyomavirus 5 (BatPyV-5) and Pan troglodytes verus polyomavirus 3 and 4 (PtroPyV3 and PtroPyV4), sharing 67–68% and 56–57% with them, respectively. ML trees were then established based on the amino acid sequence of VP1 and VP2, respectively, from the representative strains in genus Deltapolyomavirus and genus Alphapolyomavirus. Both trees revealed that GPPyV1 clustered within the clade of genus Alphapolyomavirus, discordant with the tree based on LTAg (Fig. 2 B and C), suggesting this ployomavirus strain from giant panda was involved in genomic recombination which frequently occurred during polyomavirus evolution [30].
Fig. 2
Fig. 2

Amino acid-based maximum likelihood analysis of (a) the large T antigen, (b) the major capsid protein VP1, and (c) the minor capsid protein VP2. The polyomavirus identified in this study was labeled with a red dot

Discussion

Recently, the ICTV Polyomaviridae Study Group designed the new criteria for definition of a new polyomavirus species [3], which includes four major points: i) the complete genome sequence is available in public databases and published; ii) the genome displays an organization typical for polyomaviruses; iii) sufficient information on the natural host is available; iv) the observed genetic distance to members of the most closely related species is >15% for the large T antigen (LTAg) coding sequence. Based on these criteria, GPPyV1 qualifies as a novel polyomavirus species.

In the present study, using viral metagenomic method, a new polyomavirus was detected in the nasal cavity of a dead giant panda recently released into the wild who died from unknown causes. Our PCR analysis of 13 nasal swabs and 25 fecal samples from healthy captive giant pandas showed no other positive animals, suggesting GPPyV1 is not highly prevalent in captive giant pandas. In mammals polyomaviruses infections are highly common during childhood and adolescence [31]. These persistent infections are not generally associated with acute disease in their natural non-immunocompromised hosts. On the other hand, mammalian polyomaviruses are known to induce tumors after inoculation into non-permissive laboratory rodents [32] and recently, the human polyomavirus, Merkel cell polyomavirus, has been linked to the development of skin carcinoma [8, 33]. In this study, phylogenetic analysis based on LTAg of GPPyV1 showed it had the closest relationship with polyomaviruses from genus Deltapolyomavirus which currently includes four defined species: HPyV-6, HPyV-7, MW polyomavirus, and STL polyomavirus. HPyV-6 and HPyV-7 were mainly found on human skin, while MW polyomavirus and STL polyomavirus have been isolated out of human feces, some of which are associated with human disease, for example, HPyV-7 was associated pruritic rash and viremia in transplant recipients, while MW and STL polyomavirus were reported to be present in tonsillar tissues from children with chronic tonsillar disease [10, 34]. Using an alternative classification scheme both the LT and the VP1 proteins cluster in the Almi clade [35]. The polyomaviruses (HPyV-6, HPyV-7, MW, and STL) whose LT are most closely related to that of GPPyV1 have VP1s that cluster in a different (Wuki) clade than GPPyV1 (Almi) indicating that these genomes may be recombinant of an original virus whose VP1 gene was more related to the GPPyV1 genome described here. During the evolution of polyomavirus, recombination does not seem to occur randomly across the genome but has rearranged the early and late genomic regions of major polyomavirus lineages. For instance, a lineage comprising KIPyV, WUPyV and two related rodent polyomaviruses belongs to the clade corresponding to the genus Betapolyomavirus in LTAg phylogenetic trees, however it clusters within a lineage of the genus Deltapolyomavirus based on the phylogenetic analysis over the VP1 sequences [3537].

Conclusion

A novel polyomavirus, GPPyV1, was detected in the nasal cavity of a dead giant panda, whose complete genome was determined. Phylogenetic analysis based on the LTAg suggested GPPyV1 belonged to a putative new species within genus Deltapolyomavirus. Epidemiological results suggested GPPyV1 is also prevalent in captive giant pandas. Whether GPPyV1 cause specific disease in giant pandas remain unknown.

Abbreviations

BLAST: 

Basic Local Alignment Search Tool

GPPyV: 

giant panda polyomavirus

ICTV: 

the International Committee on Taxonomy of Viruses

LTAg: 

large T antigen

ORF: 

open reading frame

PCR: 

polymerase chain reaction

STAg: 

small T antigen

Declarations

Acknowledgements

We would like to thank Zhi Yang, Peng Chen, Yi Geng, Hao Hu, Kan Zhang, Xiaoqing Li, Xu Shi, Jiahua Ou, Hong Liu, Yanshan Zhou, Jiabin Liu, Rui Ma, Chao Chen, Zusheng Li, and our colleagues at Panda Center for their assistance during this study.

Funding

This work was partly supported by National Key Research and Development Programs of China No. 2017YFC1200201 and No.2016YFC0503200, National Natural Science Foundation of China No. 31372223 and 31772484, Jiangsu Provincial Key Research and Development Projects No. BE2017693, Sichuan Youth Science and Technology Foundation No. 2017JQ0026, Chengdu Giant Panda Breeding Research Foundation No. CPF 2013–17, 2014–11 and 2015–19, Chengdu Science and Technology Bureau (2015-HM01-00265-SF), and Blood Systems Research Institute.

Availability of data and materials

The novel polyomavirus genome of GPPyV1 and sequence generated by PCR screening were deposited in GenBank under the following accession numbers: KY612371 and MF370864.

Authors’ contributions

WZ and RH conceived the study. DQ, TS and WZ performed most of the experiments. WZ wrote the paper. All authors participated the experiments and read and approved the final manuscript.

Ethics approval and consent to participate

Sample collection and all experiments in the present study were performed with Ethical Approval given by Ethics Committee of Jiangsu University and the reference number is No. UJS2016022.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

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Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Sichuan Key Laboratory of Conservation Biology for Endangered Wildlife, Chengdu Research Base of Giant Panda Breeding, Chengdu, Sichuan, 610081, China
(2)
Department of Microbiology, School of Medicine, Jiangsu University, Zhenjiang, Jiangsu, 212013, China
(3)
Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai, 200241, China
(4)
Blood Systems Research Institute, San Francisco, California, 94118, USA
(5)
Liziping Nature Reserve, YaAn, Sichuan Province, Sichuan, 625499, China

References

  1. DeCaprio JA, Garcea RL. A cornucopia of human polyomaviruses. Nature Reviews. Microbiology. 2013;11:264–76.PubMedPubMed CentralGoogle Scholar
  2. Gerits N, Moens U. Agnoprotein of mammalian polyomaviruses. Virology. 2012;432:316–26.View ArticlePubMedGoogle Scholar
  3. Calvignac-Spencer S, Feltkamp MCW, Daugherty MD, Moens U, Ramqvist T, Johne R, Ehlers B, Ehlers B. A taxonomy update for the family Polyomaviridae. Arch Virol. 2016;161:1739–50.View ArticlePubMedGoogle Scholar
  4. Yogo Y, Sugimoto C, Zhong S, Homma Y. Evolution of the BK polyomavirus: epidemiological, anthropological and clinical implications. Rev Med Virol. 2009;19:185–99.View ArticlePubMedGoogle Scholar
  5. Abend JR, Jiang M, Imperiale MJ. BK virus and human cancer: innocent until proven guilty. Semin Cancer Biol. 2009;19:252–60.View ArticlePubMedPubMed CentralGoogle Scholar
  6. Gardner SD, Field AM, Coleman DV, Hulme B. New human papovavirus (B.K.) isolated from urine after renal transplantation. Lancet (London, England). 1971;1:1253–7.View ArticleGoogle Scholar
  7. Padgett BL, Walker DL, ZuRhein GM, Eckroade RJ, Dessel BH. Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. Lancet (London, England). 1971;1:1257–60.View ArticleGoogle Scholar
  8. Feng H, Shuda M, Chang Y, Moore PS. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science (New York, NY). 2008;319:1096–100.View ArticleGoogle Scholar
  9. van der Meijden E, Janssens RWA, Lauber C, Bouwes Bavinck JN, Gorbalenya AE, Feltkamp MCW. Discovery of a new human polyomavirus associated with trichodysplasia spinulosa in an immunocompromized patient. PLoS Pathog. 2010;6:e1001024.View ArticlePubMedPubMed CentralGoogle Scholar
  10. Ho J, Jedrych JJ, Feng H, Natalie AA, Grandinetti L, Mirvish E, Crespo MM, Yadav D, Fasanella KE, Proksell S, Kuan S-F, Pastrana DV, Buck CB, Shuda Y, Moore PS, Chang Y. Human polyomavirus 7-associated pruritic rash and viremia in transplant recipients. J Infect Dis. 2015;211:1560–5.View ArticlePubMedGoogle Scholar
  11. Siebrasse EA, Nguyen NL, Willby MJ, Erdman DD, Menegus MA, Wang D. Multiorgan WU Polyomavirus infection in bone marrow transplant recipient. Emerg Infect Dis. 2016;22:24–31.View ArticlePubMedPubMed CentralGoogle Scholar
  12. Toptan T, Yousem SA, Ho J, Matsushima Y, Stabile LP, Fernández-Figueras M-T, Bhargava R, Ryo A, Moore PS, Chang Y. Survey for human polyomaviruses in cancer. JCI Insight. 2016;1Google Scholar
  13. Johne R, Enderlein D, Nieper H, Müller H. Novel polyomavirus detected in the feces of a chimpanzee by nested broad-spectrum PCR. J Virol. 2005;79:3883–7.View ArticlePubMedPubMed CentralGoogle Scholar
  14. Misra V, Dumonceaux T, Dubois J, Willis C, Nadin-Davis S, Severini A, Wandeler A, Lindsay R, Artsob H. Detection of polyoma and corona viruses in bats of Canada. The Journal of general virology. 2009;90(Pt 8):2015–22.View ArticlePubMedGoogle Scholar
  15. Groenewoud MJ, Fagrouch Z, van Gessel S, Niphuis H, Bulavaite A, Warren KS, Heeney JL, Verschoor EJ. Characterization of novel polyomaviruses from Bornean and Sumatran orang-utans. The Journal of general virology. 2010;91(Pt 3):653–8.View ArticlePubMedGoogle Scholar
  16. Rigatti LH, Toptan T, Newsome JT, Moore PS, Chang Y. Identification and characterization of novel rat Polyomavirus 2 in a Colony of X-SCID rats by P-PIT assay. mSphere. 2016;1:e00334–16.View ArticlePubMedPubMed CentralGoogle Scholar
  17. Van Borm S, Rosseel T, Behaeghel I, Saulmont M, Delooz L, Petitjean T, Mathijs E, Vandenbussche F. Complete genome sequence of bovine Polyomavirus type 1 from aborted cattle, isolated in Belgium in 2014. Genome Announcements. 2016;4:e01646–15.PubMedPubMed CentralGoogle Scholar
  18. van Persie J, Buitendijk H, Fagrouch Z, Bogers W, Haaksma T, Kondova I, Verschoor EJ. Complete genome sequence of a novel chimpanzee Polyomavirus from a western common chimpanzee. Genome Announcements. 2016;4:e01406–15.View ArticlePubMedPubMed CentralGoogle Scholar
  19. Nainys J, Timinskas A, Schneider J, Ulrich RG, Gedvilaite A. Identification of two novel members of the tentative genus Wukipolyomavirus in wild rodents. PLoS One. 2015;10:e0140916.View ArticlePubMedPubMed CentralGoogle Scholar
  20. Murray ZL, Hall RJ, Moore NE, McInnes K, Tompkins DM, Wang J, White DJ. Discovery of novel virus sequences in an isolated and threatened bat species, the New Zealand lesser short-tailed bat (Mystacina Tuberculata). J Gen Virol. 2015;96:2442–52.View ArticlePubMedPubMed CentralGoogle Scholar
  21. Chambers M, Murphy AA, Palser AL, Grierson S, Hill SC, Boschiroli M-L, Bhuachalla DN, Pybus OG, Cotten M, Lesellier S, Richomme C, Kellam P, Jarvis MA, Benson P, Ehlers B, Gormley E: Discovery of a polyomavirus in European badgers (Meles Meles) and the evolution of host range in the family Polyomaviridae. J Gen Virol 2015, 96:1411–1422.Google Scholar
  22. Varsani A, Porzig EL, Jennings S, Kraberger S, Farkas K, Julian L, Massaro M, Ballard G, Ainley DG. Identification of an avian polyomavirus associated with Adelie penguins (Pygoscelis Adeliae). J Gen Virol. 2015;96(Pt_4):851–7.View ArticlePubMedGoogle Scholar
  23. Stevens H, Bertelsen MF, Sijmons S, Van Ranst M, Maes P. Characterization of a novel polyomavirus isolated from a fibroma on the trunk of an African elephant (Loxodonta Africana). PLoS One. 2013;8:e77884.View ArticlePubMedPubMed CentralGoogle Scholar
  24. Dela Cruz FN, Giannitti F, Li L, Woods LW, Del Valle L, Delwart E, Pesavento PA. Novel polyomavirus associated with brain tumors in free-ranging raccoons, western United States. Emerg Infect Dis. 2013;19:77–84.View ArticlePubMedPubMed CentralGoogle Scholar
  25. Zhang W, Li L, Deng X, Kapusinszky B, Pesavento PA, Delwart E. Faecal virome of cats in an animal shelter. The Journal of general virology. 2014;95(Pt 11):2553–64.View ArticlePubMedPubMed CentralGoogle Scholar
  26. Zhang W, Li L, Deng X, Blümel J, Nübling CM, Hunfeld A, Baylis SA, Delwart E. Viral nucleic acids in human plasma pools. Transfusion. 2016;56:2248–55.View ArticlePubMedGoogle Scholar
  27. Liu Z, Yang S, Wang Y, Shen Q, Yang Y, Deng X, Zhang W, Delwart E. Identification of a novel human papillomavirus by metagenomic analysis of vaginal swab samples from pregnant women. Virol J. 2016;13:122.View ArticlePubMedPubMed CentralGoogle Scholar
  28. Deng X, Naccache SN, Ng T, Federman S, Li L, Chiu CY, Delwart EL. An ensemble strategy that significantly improves de novo assembly of microbial genomes from metagenomic next-generation sequencing data. Nucleic Acids Res. 2015;Google Scholar
  29. Siebrasse EA, Reyes A, Lim ES, Zhao G, Mkakosya RS, Manary MJ, Gordon JI, Wang D. Identification of MW polyomavirus, a novel polyomavirus in human stool. J Virol. 2012;86:10321–6.View ArticlePubMedPubMed CentralGoogle Scholar
  30. Moens U, Krumbholz A, Ehlers B, Zell R, Johne R, Calvignac-Spencer S, Lauber C. Biology, evolution, and medical importance of polyomaviruses: an update. Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases. 2017;54:18–38.View ArticlePubMedGoogle Scholar
  31. Egli A, Infanti L, Dumoulin A, Buser A, Samaridis J, Stebler C, Gosert R, Hirsch HH. Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors. J Infect Dis. 2009;199:837–46.View ArticlePubMedGoogle Scholar
  32. GIRARDI AJ, SWEET BH, SLOTNICK VB, HILLEMAN MR. Development of tumors in hamsters inoculated in the neonatal period with vacuolating virus, SV-40. Proceedings of the Society for Experimental Biology and Medicine Society for Experimental Biology and Medicine (New York, NY). 1962;109:649–60.View ArticleGoogle Scholar
  33. Spurgeon ME, Lambert PF. Merkel cell polyomavirus: a newly discovered human virus with oncogenic potential. Virology. 2013;435:118–30.View ArticlePubMedPubMed CentralGoogle Scholar
  34. Peng J, Li K, Zhang C, Jin Q: MW polyomavirus and STL polyomavirus present in tonsillar tissues from children with chronic tonsillar disease. Clinical Microbiology and Infection 2016, 22:97.e1–97.e3.Google Scholar
  35. Buck CB, Van Doorslaer K, Peretti A, Geoghegan EM, Tisza MJ, An P, Katz JP, Pipas JM, McBride AA, Camus AC, McDermott AJ, Dill JA, Delwart E, Ng TFF, Farkas K, Austin C, Kraberger S, Davison W, Pastrana DV, Varsani A. The ancient evolutionary history of Polyomaviruses. PLoS Pathog. 2016;12:e1005574.View ArticlePubMedPubMed CentralGoogle Scholar
  36. Lim ES, Reyes A, Antonio M, Saha D, Ikumapayi UN, Adeyemi M, Stine OC, Skelton R, Brennan DC, Mkakosya RS, Manary MJ, Gordon JI, Wang D. Discovery of STL polyomavirus, a polyomavirus of ancestral recombinant origin that encodes a unique T antigen by alternative splicing. Virology. 2013;436:295–303.View ArticlePubMedGoogle Scholar
  37. Tao Y, Shi M, Conrardy C, Kuzmin IV, Recuenco S, Agwanda B, Alvarez DA, Ellison JA, Gilbert AT, Moran D, Niezgoda M, Lindblade KA, Holmes EC, Breiman RF, Rupprecht CE, Tong S. Discovery of diverse polyomaviruses in bats and the evolutionary history of the Polyomaviridae. The Journal of general virology. 2013;94(Pt 4):738–48.View ArticlePubMedGoogle Scholar

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