Skip to main content
Top
Published in: Virology Journal 1/2018

Open Access 01-12-2018 | Research

Plasma virome of cattle from forest region revealed diverse small circular ssDNA viral genomes

Authors: Hao Wang, Shouxin Li, Asif Mahmood, Shixing Yang, Xiaochun Wang, Quan Shen, Tongling Shan, Xutao Deng, Jingjiao Li, Xiuguo Hua, Li Cui, Eric Delwart, Wen Zhang

Published in: Virology Journal | Issue 1/2018

Login to get access

Abstract

Background

Free-range cattle are common in the Northeast China area, which have close contact with farmers and may carry virus threatening to cattle and farmers.

Methods

Using viral metagenomics we analyzed the virome in plasma samples collected from 80 cattle from the forested region of Northeast China.

Results

The virome of cattle plasma is composed of the viruses belonging to the families including Parvoviridae, Papillomaviridae, Picobirnaviridae, and divergent viral genomes showing sequence similarity to circular Rep-encoding single stranded (CRESS) DNA viruses. Five such CRESS-DNA genomes were full characterized, with Rep sequences related to circovirus and gemycircularvirus. Three bovine parvoviruses belonging to two different genera were also characterized.

Conclusion

The virome in plasma samples of cattle from the forested region of Northeast China was revealed, which further characterized the diversity of viruses in cattle plasma.
Appendix
Available only for authorised users
Literature
1.
go back to reference Delwart E, Li L. Rapidly expanding genetic diversity and host range of the Circoviridae viral family and other rep encoding small circular ssDNA genomes. Virus Res. 2012;164:114–21.CrossRefPubMed Delwart E, Li L. Rapidly expanding genetic diversity and host range of the Circoviridae viral family and other rep encoding small circular ssDNA genomes. Virus Res. 2012;164:114–21.CrossRefPubMed
2.
go back to reference Rosario K, Duffy S, Breitbart M. A field guide to eukaryotic circular single-stranded DNA viruses: insights gained from metagenomics. Arch Virol. 2012;157:1851–71.CrossRefPubMed Rosario K, Duffy S, Breitbart M. A field guide to eukaryotic circular single-stranded DNA viruses: insights gained from metagenomics. Arch Virol. 2012;157:1851–71.CrossRefPubMed
3.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
4.
go back to reference Dunlap DS, Ng TFF, Rosario K, Barbosa JG, Greco AM, Breitbart M, Hewson I. Molecular and microscopic evidence of viruses in marine copepods. Proc Natl Acad Sci. 2013;110:1375–80.CrossRefPubMedPubMedCentral Dunlap DS, Ng TFF, Rosario K, Barbosa JG, Greco AM, Breitbart M, Hewson I. Molecular and microscopic evidence of viruses in marine copepods. Proc Natl Acad Sci. 2013;110:1375–80.CrossRefPubMedPubMedCentral
5.
go back to reference Ng T, Alavandi S, Varsani A, Burghart S, Breitbart M. 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 Org. 2013;105:237–42.CrossRefPubMed Ng T, Alavandi S, Varsani A, Burghart S, Breitbart M. 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 Org. 2013;105:237–42.CrossRefPubMed
6.
go back to reference Yu X, Li B, Fu Y, Jiang D, Ghabrial SA, Li G, Peng Y, Xie J, Cheng J, Huang J, Yi X. A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci U S A. 2010;107:8387–92.CrossRefPubMedPubMedCentral Yu X, Li B, Fu Y, Jiang D, Ghabrial SA, Li G, Peng Y, Xie J, Cheng J, Huang J, Yi X. A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci U S A. 2010;107:8387–92.CrossRefPubMedPubMedCentral
7.
go back to reference Zawar-Reza P, Argüello-Astorga GR, Kraberger S, Julian L, Stainton D, Broady PA, Varsani A. Diverse small circular single-stranded DNA viruses identified in a freshwater pond on the McMurdo ice shelf (Antarctica). Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases. 2014;26:132–8.CrossRefPubMed Zawar-Reza P, Argüello-Astorga GR, Kraberger S, Julian L, Stainton D, Broady PA, Varsani A. Diverse small circular single-stranded DNA viruses identified in a freshwater pond on the McMurdo ice shelf (Antarctica). Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases. 2014;26:132–8.CrossRefPubMed
8.
go back to reference Rosario K, Dayaram A, Marinov M, Ware J, Kraberger S, Stainton D, Breitbart M, Varsani A. Diverse circular ssDNA viruses discovered in dragonflies (Odonata: Epiprocta). The Journal of general virology. 2012;93(Pt 12):2668–81.CrossRefPubMed Rosario K, Dayaram A, Marinov M, Ware J, Kraberger S, Stainton D, Breitbart M, Varsani A. Diverse circular ssDNA viruses discovered in dragonflies (Odonata: Epiprocta). The Journal of general virology. 2012;93(Pt 12):2668–81.CrossRefPubMed
9.
go back to reference Dayaram A, Potter KA, Moline AB, Rosenstein DD, Marinov M, Thomas JE, Breitbart M, Rosario K, Argüello-Astorga GR, Varsani A. High global diversity of cycloviruses amongst dragonflies. The Journal of general virology. 2013;94(Pt 8):1827–40.CrossRefPubMed Dayaram A, Potter KA, Moline AB, Rosenstein DD, Marinov M, Thomas JE, Breitbart M, Rosario K, Argüello-Astorga GR, Varsani A. High global diversity of cycloviruses amongst dragonflies. The Journal of general virology. 2013;94(Pt 8):1827–40.CrossRefPubMed
10.
go back to reference Rosario K, Seah YM, Marr C, Varsani A, Kraberger S, Stainton D, Moriones E, Polston JE, Duffy S, Breitbart M. Vector-Enabled Metagenomic (VEM) Surveys Using Whiteflies (Aleyrodidae) Reveal Novel Begomovirus Species in the New and Old Worlds. Viruses. 2015;7(10):5553–70. Rosario K, Seah YM, Marr C, Varsani A, Kraberger S, Stainton D, Moriones E, Polston JE, Duffy S, Breitbart M. Vector-Enabled Metagenomic (VEM) Surveys Using Whiteflies (Aleyrodidae) Reveal Novel Begomovirus Species in the New and Old Worlds. Viruses. 2015;7(10):5553–70.
11.
go back to reference Sikorski A, Massaro M, Kraberger S, Young LM, Smalley D, Martin DP, Varsani A. Novel myco-like DNA viruses discovered in the faecal matter of various animals. Virus Res. 2013;177:209–16.CrossRefPubMed Sikorski A, Massaro M, Kraberger S, Young LM, Smalley D, Martin DP, Varsani A. Novel myco-like DNA viruses discovered in the faecal matter of various animals. Virus Res. 2013;177:209–16.CrossRefPubMed
12.
go back to reference Smits SL, Zijlstra EE, van Hellemond JJ, Schapendonk CME, Bodewes R, Schürch AC, Haagmans BL, Osterhaus ADME: Novel cyclovirus in human cerebrospinal fluid, Malawi, 2010–2011. Emerging infectious diseases. 2013;19:1511–13. Smits SL, Zijlstra EE, van Hellemond JJ, Schapendonk CME, Bodewes R, Schürch AC, Haagmans BL, Osterhaus ADME: Novel cyclovirus in human cerebrospinal fluid, Malawi, 2010–2011. Emerging infectious diseases. 2013;19:1511–13.
15.
go back to reference Reuter G, Boros Á, Delwart E, Pankovics P. Novel circular single-stranded DNA virus from turkey faeces. Arch Virol. 2014;159:2161–4.CrossRefPubMed Reuter G, Boros Á, Delwart E, Pankovics P. Novel circular single-stranded DNA virus from turkey faeces. Arch Virol. 2014;159:2161–4.CrossRefPubMed
16.
go back to reference Cheung AK, Ng TF, Lager KM, Bayles DO, Alt DP, Delwart EL, Pogranichniy RM, Kehrli ME. A divergent clade of circular single-stranded DNA viruses from pig feces. Arch Virol. 2013;158:2157–62.CrossRefPubMedPubMedCentral Cheung AK, Ng TF, Lager KM, Bayles DO, Alt DP, Delwart EL, Pogranichniy RM, Kehrli ME. A divergent clade of circular single-stranded DNA viruses from pig feces. Arch Virol. 2013;158:2157–62.CrossRefPubMedPubMedCentral
17.
go back to reference Tijssen P, Pénzes JJ, Yu Q, Pham HT, Bergoin M. Diversity of small, single-stranded DNA viruses of invertebrates and their chaotic evolutionary past. J Invertebr Pathol. 2016;140:83–96.CrossRefPubMed Tijssen P, Pénzes JJ, Yu Q, Pham HT, Bergoin M. Diversity of small, single-stranded DNA viruses of invertebrates and their chaotic evolutionary past. J Invertebr Pathol. 2016;140:83–96.CrossRefPubMed
18.
go back to reference Breitbart M, Delwart E, Rosario K, Segalés J, Varsani A, Ictv Report Consortium: ICTV Virus Taxonomy Profile: Circoviridae. The Journal of general virology. 2017;98(8):1997–8. Breitbart M, Delwart E, Rosario K, Segalés J, Varsani A, Ictv Report Consortium: ICTV Virus Taxonomy Profile: Circoviridae. The Journal of general virology. 2017;98(8):1997–8.
19.
go back to reference Li L, Deng X, Mee ET, Collot-Teixeira S, Anderson R, Schepelmann S, Minor PD, Delwart E. Comparing viral metagenomics methods using a highly multiplexed human viral pathogens reagent. J Virol Methods. 2014;213C:139–46. Li L, Deng X, Mee ET, Collot-Teixeira S, Anderson R, Schepelmann S, Minor PD, Delwart E. Comparing viral metagenomics methods using a highly multiplexed human viral pathogens reagent. J Virol Methods. 2014;213C:139–46.
20.
go back to reference 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 Research 2015. 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 Research 2015.
21.
go back to reference Zhang W, Yang S, Shan T, Hou R, Liu Z, Li W, Guo L, Wang Y, Chen P, Wang X, Feng F, Wang H, Chen C, Shen Q, Zhou C, Hua X, Cui L, Deng X, Zhang Z, Qi D, Delwart E. Virome comparisons in wild-diseased and healthy captive giant pandas. Microbiome. 2017;5:90.CrossRefPubMedPubMedCentral Zhang W, Yang S, Shan T, Hou R, Liu Z, Li W, Guo L, Wang Y, Chen P, Wang X, Feng F, Wang H, Chen C, Shen Q, Zhou C, Hua X, Cui L, Deng X, Zhang Z, Qi D, Delwart E. Virome comparisons in wild-diseased and healthy captive giant pandas. Microbiome. 2017;5:90.CrossRefPubMedPubMedCentral
23.
go back to reference Skewes-Cox P, Sharpton TJ, Pollard KS, DeRisi JL. Profile hidden Markov models for the detection of viruses within metagenomic sequence data. PLoS One. 2014;9:e105067.CrossRefPubMedPubMedCentral Skewes-Cox P, Sharpton TJ, Pollard KS, DeRisi JL. Profile hidden Markov models for the detection of viruses within metagenomic sequence data. PLoS One. 2014;9:e105067.CrossRefPubMedPubMedCentral
25.
go back to reference Eddy SR. A new generation of homology search tools based on probabilistic inference. Genome informatics International Conference on Genome Informatics. 2009;23:205–11.PubMed Eddy SR. A new generation of homology search tools based on probabilistic inference. Genome informatics International Conference on Genome Informatics. 2009;23:205–11.PubMed
26.
27.
go back to reference Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG, Clustal W, Clustal X. Version 2.0. Bioinformatics (Oxford, England). 2007;23:2947–8.CrossRef Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG, Clustal W, Clustal X. Version 2.0. Bioinformatics (Oxford, England). 2007;23:2947–8.CrossRef
28.
go back to reference Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–9.CrossRefPubMedPubMedCentral Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–9.CrossRefPubMedPubMedCentral
29.
go back to reference 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;43:e46.CrossRefPubMedPubMedCentral 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;43:e46.CrossRefPubMedPubMedCentral
30.
go back to reference Krupovic M, Ghabrial SA, Jiang D, Varsani A. Genomoviridae: a new family of widespread single-stranded DNA viruses. Arch Virol. 2016;161:2633–43.CrossRefPubMed Krupovic M, Ghabrial SA, Jiang D, Varsani A. Genomoviridae: a new family of widespread single-stranded DNA viruses. Arch Virol. 2016;161:2633–43.CrossRefPubMed
31.
go back to reference TFF N, Zhang W, Sachsenröder J, Kondov NO, da Costa AC, Vega E, Holtz LR, Wu G, Wang D, Stine CO, Antonio M, Mulvaney US, Muench MO, Deng X, Ambert-Balay K, Pothier P, Vinjé J, Delwart E. A diverse group of small circular ssDNA viral genomes in human and non-human primate stools. Virus Evolution. 2015;1:vev017.CrossRef TFF N, Zhang W, Sachsenröder J, Kondov NO, da Costa AC, Vega E, Holtz LR, Wu G, Wang D, Stine CO, Antonio M, Mulvaney US, Muench MO, Deng X, Ambert-Balay K, Pothier P, Vinjé J, Delwart E. A diverse group of small circular ssDNA viral genomes in human and non-human primate stools. Virus Evolution. 2015;1:vev017.CrossRef
32.
go back to reference Kapusinszky B, Ardeshir A, Mulvaney U, Deng X, Delwart E. Case control comparison of enteric viromes in captive rhesus macaques with acute or idiopathic chronic diarrhea. J Virol. 2017;91(18):JVI.00952–17. Kapusinszky B, Ardeshir A, Mulvaney U, Deng X, Delwart E. Case control comparison of enteric viromes in captive rhesus macaques with acute or idiopathic chronic diarrhea. J Virol. 2017;91(18):JVI.00952–17.
33.
go back to reference Cheung AK, Ng TFF, Lager KM, Alt DP, Delwart E, Pogranichniy RM. Identification of several clades of novel single-stranded circular DNA viruses with conserved stem-loop structures in pig feces. Arch Virol. 2015;160:353–8.CrossRefPubMed Cheung AK, Ng TFF, Lager KM, Alt DP, Delwart E, Pogranichniy RM. Identification of several clades of novel single-stranded circular DNA viruses with conserved stem-loop structures in pig feces. Arch Virol. 2015;160:353–8.CrossRefPubMed
34.
go back to reference Steel O, Kraberger S, Sikorski A, Young LM, Catchpole RJ, Stevens AJ, Ladley JJ, Coray DS, Stainton D, Dayaram A, Julian L, van Bysterveldt K, Varsani A. Circular replication-associated protein encoding DNA viruses identified in the faecal matter of various animals in New Zealand. Infect Genet Evol. 2016;43:151–64.CrossRefPubMed Steel O, Kraberger S, Sikorski A, Young LM, Catchpole RJ, Stevens AJ, Ladley JJ, Coray DS, Stainton D, Dayaram A, Julian L, van Bysterveldt K, Varsani A. Circular replication-associated protein encoding DNA viruses identified in the faecal matter of various animals in New Zealand. Infect Genet Evol. 2016;43:151–64.CrossRefPubMed
35.
go back to reference Ng TFF, Kondov NO, Deng X, Van Eenennaam A, Neibergs HL, Delwart E, Metagenomics A. Case-control study to identify viruses associated with bovine respiratory disease. J Virol. 2015;89:5340–9.CrossRefPubMedPubMedCentral Ng TFF, Kondov NO, Deng X, Van Eenennaam A, Neibergs HL, Delwart E, Metagenomics A. Case-control study to identify viruses associated with bovine respiratory disease. J Virol. 2015;89:5340–9.CrossRefPubMedPubMedCentral
36.
go back to reference Woode GN, Reed DE, Runnels PL, Herrig MA, Hill HT. Studies with an unclassified virus isolated from diarrheic calves. Vet Microbiol. 1982;7:221–40.CrossRefPubMed Woode GN, Reed DE, Runnels PL, Herrig MA, Hill HT. Studies with an unclassified virus isolated from diarrheic calves. Vet Microbiol. 1982;7:221–40.CrossRefPubMed
37.
go back to reference Sadeghi M, Kapusinszky B, Yugo DM, Phan TG, Deng X, Kanevsky I, Opriessnig T, Woolums AR, Hurley DJ, Meng X-J, Delwart E. Virome of US bovine calf serum. Biologicals. 2017;46:64–7.CrossRefPubMed Sadeghi M, Kapusinszky B, Yugo DM, Phan TG, Deng X, Kanevsky I, Opriessnig T, Woolums AR, Hurley DJ, Meng X-J, Delwart E. Virome of US bovine calf serum. Biologicals. 2017;46:64–7.CrossRefPubMed
38.
go back to reference Toohey-Kurth K, Sibley SD, Goldberg TL. Metagenomic assessment of adventitious viruses in commercial bovine sera. Biologicals. 2017;47:64–8.CrossRefPubMed Toohey-Kurth K, Sibley SD, Goldberg TL. Metagenomic assessment of adventitious viruses in commercial bovine sera. Biologicals. 2017;47:64–8.CrossRefPubMed
39.
go back to reference Ogawa T, Tomita Y, Okada M, Shinozaki K, Kubonoya H, Kaiho I, Shirasawa H. Broad-spectrum detection of papillomaviruses in bovine teat papillomas and healthy teat skin. J Gen Virol. 2004;85:2191–7.CrossRefPubMed Ogawa T, Tomita Y, Okada M, Shinozaki K, Kubonoya H, Kaiho I, Shirasawa H. Broad-spectrum detection of papillomaviruses in bovine teat papillomas and healthy teat skin. J Gen Virol. 2004;85:2191–7.CrossRefPubMed
40.
go back to reference Ganesh B, Bányai K, Martella V, Jakab F, Masachessi G, Kobayashi N. Picobirnavirus infections: viral persistence and zoonotic potential. Rev Med Virol. 2012;22:245–56.CrossRefPubMed Ganesh B, Bányai K, Martella V, Jakab F, Masachessi G, Kobayashi N. Picobirnavirus infections: viral persistence and zoonotic potential. Rev Med Virol. 2012;22:245–56.CrossRefPubMed
42.
go back to reference Colson P, Fancello L, Gimenez G, Armougom F, Desnues C, Fournous G, Yoosuf N, Million M, La Scola B, Raoult D. Evidence of the megavirome in humans. J Clin Virol. 2013;57:191–200.CrossRefPubMed Colson P, Fancello L, Gimenez G, Armougom F, Desnues C, Fournous G, Yoosuf N, Million M, La Scola B, Raoult D. Evidence of the megavirome in humans. J Clin Virol. 2013;57:191–200.CrossRefPubMed
43.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
Metadata
Title
Plasma virome of cattle from forest region revealed diverse small circular ssDNA viral genomes
Authors
Hao Wang
Shouxin Li
Asif Mahmood
Shixing Yang
Xiaochun Wang
Quan Shen
Tongling Shan
Xutao Deng
Jingjiao Li
Xiuguo Hua
Li Cui
Eric Delwart
Wen Zhang
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2018
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-018-0923-9

Other articles of this Issue 1/2018

Virology Journal 1/2018 Go to the issue