Abstract
The virome in genital tract secretion samples collected from 80 dairy cattle in Shanghai, China, was characterized. Viruses detected included members of the families Papillomaviridae, Polyomaviridae, Hepeviridae, Parvoviridae, Astroviridae, Picornaviridae, and Picobirnaviridae. A member of a new species within the genus Dyoxipapillomavirus and six circular Rep-encoding single-stranded DNA (ssDNA) (CRESS-DNA) viral genomes were fully sequenced and phylogenetically analyzed. The prevalence of bovine polyomaviruses 1 and 2 was measured by PCR to be 10% (8/80) and 6.25% (5/80), respectively. PCR screening also indicated that the novel papillomavirus ujs-21015 and bovine herpesvirus 6 were present in three and two out of the 80 samples, respectively.
Similar content being viewed by others
Reference
Nekouei O, VanLeeuwen J, Stryhn H et al (2016) Lifetime effects of infection with bovine leukemia virus on longevity and milk production of dairy cows. Prev Vet Med 133:1–9. https://doi.org/10.1016/j.prevetmed.2016.09.011
Gethmann J, Homeier T, Holsteg M et al (2015) BVD-2 outbreak leads to high losses in cattle farms in Western Germany. Heliyon 1:e00019. https://doi.org/10.1016/j.heliyon.2015.e00019
Favier PA, Marin MS, Pérez SE (2012) Role of bovine herpesvirus type 5 (BoHV-5) in diseases of cattle. Recent findings on BoHV-5 association with genital disease. Open Vet J 2:46–53
Sharma H, Tal R, Clark NA, Segars JH (2014) Microbiota and pelvic inflammatory disease. Semin Reprod Med 32:43–49. https://doi.org/10.1055/s-0033-1361822
Hou P, Zhao G, Wang H, He H (2018) Prevalence of bovine viral diarrhea virus in dairy cattle herds in eastern China. Trop Anim Health Prod. https://doi.org/10.1007/s11250-018-1751-z
Hou P, Wang H, Zhao G et al (2017) Rapid detection of infectious bovine Rhinotracheitis virus using recombinase polymerase amplification assays. BMC Vet Res 13:386. https://doi.org/10.1186/s12917-017-1284-0
Yang Y, Fan W, Mao Y et al (2016) Bovine leukemia virus infection in cattle of China: Association with reduced milk production and increased somatic cell score. J Dairy Sci 99:3688–3697. https://doi.org/10.3168/jds.2015-10580
Chang J, Wang Q, Wang F et al (2014) Prevalence and genetic diversity of bovine kobuvirus in China. Arch Virol 159:1505–1510. https://doi.org/10.1007/s00705-013-1961-7
Zhang W, Hu J, Yan S et al (2015) Sequence and Structural Analyses of the Complete Genome of Bovine Papillomavirus 2 Genotype Aks-01 Strain from Skin Samples of Cows in Southern Xinjiang, China. Bing Du Xue Bao (Chinese J Virol) 31:370–378
Lu G, Jia K, Ping X et al (2018) Novel bovine hepacivirus in dairy cattle, China. Emerg Microbes Infect 7:54. https://doi.org/10.1038/s41426-018-0055-8
Wang H, Li S, Mahmood A et al (2018) Plasma virome of cattle from forest region revealed diverse small circular ssDNA viral genomes. Virol J 15:11. https://doi.org/10.1186/s12985-018-0923-9
Li L, Deng X, Mee ET et al (2014) Comparing viral metagenomics methods using a highly multiplexed human viral pathogens reagent. J Virol Methods 213C:139–146. https://doi.org/10.1016/j.jviromet.2014.12.002
Zhang W, Li L, Deng X et al (2016) Viral nucleic acids in human plasma pools. Transfusion 56:2248–2255. https://doi.org/10.1111/trf.13692
Deng X, Naccache SN, Ng T et al (2015) An ensemble strategy that significantly improves de novo assembly of microbial genomes from metagenomic next-generation sequencing data. Nucleic Acids Res. https://doi.org/10.1093/nar/gkv002
Zhang W, Yang S, Shan T et al (2017) Virome comparisons in wild-diseased and healthy captive giant pandas. Microbiome 5:90. https://doi.org/10.1186/s40168-017-0308-0
Larkin MA, Blackshields G, Brown NP et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404
Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121
Munday JS, Thomson N, Dunowska M, Knight CG, Laurie REHS (2015) Genomic characterisation of the feline sarcoid-associated papillomavirus and proposed classification as Bos taurus papillomavirus type 14.—PubMed—NCBI. Vet Microbiol 177:289–295
Steel O, Kraberger S, Sikorski A et al (2016) Circular replication-associated protein encoding DNA viruses identified in the faecal matter of various animals in New Zealand. Infect Genet Evol 43:151–164. https://doi.org/10.1016/j.meegid.2016.05.008
Woo PCY, Lau SKP, Teng JLL et al (2014) Metagenomic analysis of viromes of dromedary camel fecal samples reveals large number and high diversity of circoviruses and picobirnaviruses. Virology 471–473:117–125. https://doi.org/10.1016/j.virol.2014.09.020
Kim HK, Park SJ, Nguyen VG et al (2012) Identification of a novel single-stranded, circular DNA virus from bovine stool. J Gen Virol 93:635–639. https://doi.org/10.1099/vir.0.037838-0
Dayaram A, Potter KA, Pailes R et al (2015) Identification of diverse circular single-stranded DNA viruses in adult dragonflies and damselflies (Insecta: Odonata) of Arizona and Oklahoma, USA. Infect Genet Evol 30:278–287. https://doi.org/10.1016/j.meegid.2014.12.037
Gräfe D, Ehlers B, Mäde D et al (2017) Detection and genome characterization of bovine polyomaviruses in beef muscle and ground beef samples from Germany. Int J Food Microbiol 241:168–172. https://doi.org/10.1016/j.ijfoodmicro.2016.10.024
Peretti A, FitzGerald PC, Bliskovsky V et al (2015) Hamburger polyomaviruses. J Gen Virol 96:833–839. https://doi.org/10.1099/vir.0.000033
Jia J, Delhon G, Tulman ER et al (2014) Novel gammaherpesvirus functions encoded by bovine herpesvirus 6 (bovine lymphotropic virus). J Gen Virol 95:1790–1798. https://doi.org/10.1099/vir.0.066951-0
Munday JS (2014) Bovine and human papillomaviruses: a comparative review. Vet Pathol 51:1063–1075. https://doi.org/10.1177/0300985814537837
Elzein ETE, Sundberg JP, Housawi FM et al (1991) Genital bovine papillomavirus infection in Saudi Arabia. J Vet Diagn Invest 3:36–38. https://doi.org/10.1177/104063879100300108
Bernard H-U, Burk RD, Chen Z et al (2010) Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401:70–79. https://doi.org/10.1016/j.virol.2010.02.002
Joh J, Jenson AB, King W et al (2011) Genomic analysis of the first laboratory-mouse papillomavirus. J Gen Virol 92:692–698. https://doi.org/10.1099/vir.0.026138-0
Delwart E, Li L (2012) Rapidly expanding genetic diversity and host range of the Circoviridae viral family and other Rep encoding small circular ssDNA genomes. Virus Res 164:114–121. https://doi.org/10.1016/j.virusres.2011.11.021
Rosario K, Duffy S, Breitbart M (2012) A field guide to eukaryotic circular single-stranded DNA viruses: insights gained from metagenomics. Arch Virol 157:1851–1871. https://doi.org/10.1007/s00705-012-1391-y
Dunlap DS, Ng TFF, Rosario K et al (2013) Molecular and microscopic evidence of viruses in marine copepods. Proc Natl Acad Sci 110:1375–1380. https://doi.org/10.1073/pnas.1216595110
Ng T, Alavandi S, Varsani A et al (2013) Metagenomic identification of a nodavirus and a circular ssDNA virus in semi-purified viral nucleic acids from the hepatopancreas of healthy Farfantepenaeus duorarum shrimp. Dis Aquat Organ 105:237–242. https://doi.org/10.3354/dao02628
Yu X, Li B, Fu Y et al (2010) A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci USA 107:8387–8392. https://doi.org/10.1073/pnas.0913535107
Zawar-Reza P, Argüello-Astorga GR, Kraberger S et al (2014) Diverse small circular single-stranded DNA viruses identified in a freshwater pond on the McMurdo Ice Shelf (Antarctica). Infect Genet Evol 26:132–138. https://doi.org/10.1016/j.meegid.2014.05.018
Rosario K, Dayaram A, Marinov M et al (2012) Diverse circular ssDNA viruses discovered in dragonflies (Odonata: Epiprocta). J Gen Virol 93:2668–2681. https://doi.org/10.1099/vir.0.045948-0
Dayaram A, Potter KA, Moline AB et al (2013) High global diversity of cycloviruses amongst dragonflies. J Gen Virol 94:1827–1840. https://doi.org/10.1099/vir.0.052654-0
Rosario K, Dayaram A, Marinov M et al (2012) Diverse circular ssDNA viruses discovered in dragonflies (Odonata: Epiprocta). J Gen Virol 93:2668–2681. https://doi.org/10.1099/vir.0.045948-0
Sikorski A, Massaro M, Kraberger S et al (2013) Novel myco-like DNA viruses discovered in the faecal matter of various animals. Virus Res 177:209–216. https://doi.org/10.1016/j.virusres.2013.08.008
Smits SL, Zijlstra EE, van Hellemond JJ et al (2013) Novel cyclovirus in human cerebrospinal fluid, Malawi, 2010–2011. Emerg Infect Dis 19:44. https://doi.org/10.3201/eid1909.130404
Phan TG, Kapusinszky B, Wang C et al (2011) The fecal viral flora of wild rodents. PLoS Pathog 7:e1002218. https://doi.org/10.1371/journal.ppat.1002218
Yogo Y, Sugimoto C, Zhong S, Homma Y (2009) Evolution of the BK polyomavirus: epidemiological, anthropological and clinical implications. Rev Med Virol 19:185–199. https://doi.org/10.1002/rmv.613
Abend JR, Jiang M, Imperiale MJ (2009) BK virus and human cancer: Innocent until proven guilty. Semin Cancer Biol 19:252–260. https://doi.org/10.1016/j.semcancer.2009.02.004
Zhang W, Li L, Deng X et al (2014) What is for dinner? Viral metagenomics of US store bought beef, pork, and chicken. Virology 468-470C:303–310. https://doi.org/10.1016/j.virol.2014.08.025
Banks M, Ibata G, Murphy AM et al (2008) Bovine lymphotropic herpesvirus and non-responsive post-partum metritis in dairy herds in the UK. Vet J 176:248–250. https://doi.org/10.1016/j.tvjl.2007.02.005
Gagnon CA, Allam O, Drolet R, Tremblay D (2010) Quebec: detection of bovine lymphotropic herpesvirus DNA in tissues of a bovine aborted fetus. Can Vet J (La Rev Vet Can) 51:1021–1022
Kubiś P, Materniak M, Kuźmak J (2013) Comparison of nested PCR and qPCR for the detection and quantitation of BoHV6 DNA. J Virol Methods 194:94–101. https://doi.org/10.1016/j.jviromet.2013.08.006
Ganesh B, Masachessi G, Mladenova Z (2014) Animal picobirnavirus. Virus Dis 25:223–238. https://doi.org/10.1007/s13337-014-0207-y
Krishnamurthy SR, Wang D (2018) Extensive conservation of prokaryotic ribosomal binding sites in known and novel picobirnaviruses. Virology 516:108–114. https://doi.org/10.1016/j.virol.2018.01.006
Acknowledgments
This work was partly supported by National Key Research and Development Programs of China no. 2017YFC1200201, Jiangsu Provincial Key Research and Development Projects no. BE2017693, National Natural Science Foundation of China nos. 81741062 and 31572525, Taizhou Science and Technology Support Project no. TS201623, Key Research and Development Plan of Zhenjiang no. SH2016060, and Blood Systems Research Institute.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This study did not include experiments with human participants or animals performed by any of the authors.
Additional information
Handling Editor: Tim Skern.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ling, Y., Zhang, X., Qi, G. et al. Viral metagenomics reveals significant viruses in the genital tract of apparently healthy dairy cows. Arch Virol 164, 1059–1067 (2019). https://doi.org/10.1007/s00705-019-04158-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-019-04158-4