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Published in: Virology Journal 1/2021

Open Access 01-12-2021 | Research

Viral metagenomics reveals two novel anelloviruses in feces of experimental rats

Authors: Song-Yi Ning, Ming-Ming Zhou, Jie Yang, Jian Zeng, Jia-Ping Wang

Published in: Virology Journal | Issue 1/2021

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Abstract

Background

Rodents are widely distributed and are the natural reservoirs of a diverse group of zoonotic viruses. Thus, analyzing the viral diversity harbored by rodents could assist efforts to predict and reduce the risk of future emergence of zoonotic viral diseases. Rodents are commonly used in animal testing, particularly mice and rats. Experimental rats are important animal models, and a history of pathogenic infections in these animals will directly affect the animal trial results. The pathogenicity of Anellovirus (AV) remains poorly understood due to the lack of a suitable model cell line or animal to support the viral cycle. This study aimed to discover possible anelloviruses from the virome in feces of experimental rats by viral metagenomic technique.

Methods

Fecal samples were collected from 10 commercial SD rats and pooled into a sample pool and then subjected to libraries construction which was then sequenced on Illumina MiSeq platform. The sequenced reads were analyzed using viral metagenomic analysis pipeline and two novel anelloviruses (AVs) were identified from fecal sample of experimental rats. The prevalence of these two viruses was investigated by conventional PCR.

Results

The complete genomic sequence of these two AVs were determined and fully characterized, with strain name ratane153-zj1 and ratane153-zj2. The circular genomes of ratane153-zj1 and ratane153-zj2 are 2785 nt and 1930 nt in length, respectively, and both include three ORFs. Ratane153-zj1 closely clustered with members within the genus Wawtorquevirus and formed a separate branch based on the phylogenetic tree constructed over the amino acid sequence of ORF1 of the two AVs identified in this study and other related AVs. While the complete amino acid sequences of ORF1 of ratane153-zj2 (nt 335 to 1390) had the highest sequence identity with an unclassified AV (GenBank No. ATY37438) from Chinchilla lanigera, and they clustered with one AV (GenBank No. QYD02305) belonging to the genus Etatorquevirus from Lynx rufus. Conventional PCR with two sets of specific primers designed based on the two genomes, respectively, showed that they were detectable at a low frequency in cohorts of experimental rats.

Conclusion

Our study expanded the genome diversity of AVs and provided genetic background information of viruses existed in experimental rats.
Literature
1.
go back to reference Nishizawa T, Okamoto H, Konishi K, Yoshizawa H, Miyakawa Y, Mayumi M. A novel DNA virus (TTV) associated with elevated transaminase levels in posttransfusion hepatitis of unknown etiology. Biochem Biophys Res Commun. 1997;241:92–7.CrossRef Nishizawa T, Okamoto H, Konishi K, Yoshizawa H, Miyakawa Y, Mayumi M. A novel DNA virus (TTV) associated with elevated transaminase levels in posttransfusion hepatitis of unknown etiology. Biochem Biophys Res Commun. 1997;241:92–7.CrossRef
2.
go back to reference Miyata H, Tsunoda H, Kazi A, Yamada A, Khan MA, Murakami J, Kamahora T, Shiraki K, Hino S. Identification of a novel GC-rich 113-nucleotide region to complete the circular, single-stranded DNA genome of TT virus, the first human circovirus. J Virol. 1999;73:3582–6.CrossRef Miyata H, Tsunoda H, Kazi A, Yamada A, Khan MA, Murakami J, Kamahora T, Shiraki K, Hino S. Identification of a novel GC-rich 113-nucleotide region to complete the circular, single-stranded DNA genome of TT virus, the first human circovirus. J Virol. 1999;73:3582–6.CrossRef
3.
go back to reference Kaczorowska J, van der Hoek L. Human anelloviruses: diverse, omnipresent and commensal members of the virome. FEMS Microbiol Rev. 2020;44:305–13.CrossRef Kaczorowska J, van der Hoek L. Human anelloviruses: diverse, omnipresent and commensal members of the virome. FEMS Microbiol Rev. 2020;44:305–13.CrossRef
4.
go back to reference Nishiyama S, Dutia BM, Stewart JP, Meredith AL, Shaw DJ, Simmonds P, Sharp CP. Identification of novel anelloviruses with broad diversity in UK rodents. J Gen Virol. 2014;95:1544–53.CrossRef Nishiyama S, Dutia BM, Stewart JP, Meredith AL, Shaw DJ, Simmonds P, Sharp CP. Identification of novel anelloviruses with broad diversity in UK rodents. J Gen Virol. 2014;95:1544–53.CrossRef
5.
go back to reference Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA. Virus taxonomy: VIIIth report of the International Committee on Taxonomy of Viruses. Academic Press; 2005. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA. Virus taxonomy: VIIIth report of the International Committee on Taxonomy of Viruses. Academic Press; 2005.
6.
go back to reference Kakkola L, Hedman K, Qiu J, Pintel D. Replication of and protein synthesis by TT viruses. TT Viruses. 2009;53–64. Kakkola L, Hedman K, Qiu J, Pintel D. Replication of and protein synthesis by TT viruses. TT Viruses. 2009;53–64.
7.
go back to reference Louten J. Essential human virology. Academic Press; 2016. Louten J. Essential human virology. Academic Press; 2016.
8.
go back to reference Bédarida S, Dussol B, Signoli M, Biagini P. Analysis of Anelloviridae sequences characterized from serial human and animal biological samples. Infect Genet Evol. 2017;53:89–93.CrossRef Bédarida S, Dussol B, Signoli M, Biagini P. Analysis of Anelloviridae sequences characterized from serial human and animal biological samples. Infect Genet Evol. 2017;53:89–93.CrossRef
9.
go back to reference de Souza WM, Fumagalli MJ, de Araujo J, Sabino-Santos G Jr, Maia FGM, Romeiro MF, Modha S, Nardi MS, Queiroz LH, Durigon EL. Discovery of novel anelloviruses in small mammals expands the host range and diversity of the Anelloviridae. Virology. 2018;514:9–17.CrossRef de Souza WM, Fumagalli MJ, de Araujo J, Sabino-Santos G Jr, Maia FGM, Romeiro MF, Modha S, Nardi MS, Queiroz LH, Durigon EL. Discovery of novel anelloviruses in small mammals expands the host range and diversity of the Anelloviridae. Virology. 2018;514:9–17.CrossRef
10.
go back to reference Segalés J, Kekarainen T: Anelloviruses. Diseases of Swine 2019;453–456. Segalés J, Kekarainen T: Anelloviruses. Diseases of Swine 2019;453–456.
11.
go back to reference Bigarré L, Beven V, De Boisséson C, Grasland B, Rose N, Biagini P, Jestin A. Pig anelloviruses are highly prevalent in swine herds in France. J Gen Virol. 2005;86:631–5.CrossRef Bigarré L, Beven V, De Boisséson C, Grasland B, Rose N, Biagini P, Jestin A. Pig anelloviruses are highly prevalent in swine herds in France. J Gen Virol. 2005;86:631–5.CrossRef
12.
go back to reference Weber MN, Cibulski SP, Olegario JC, da Silva MS, Puhl DE, Mosena ACS, Alves CDBT, Paim WP, Baumbach LF, Mayer FQ, et al. Characterization of dog serum virome from Northeastern Brazil. Virology. 2018;525:192–9.CrossRef Weber MN, Cibulski SP, Olegario JC, da Silva MS, Puhl DE, Mosena ACS, Alves CDBT, Paim WP, Baumbach LF, Mayer FQ, et al. Characterization of dog serum virome from Northeastern Brazil. Virology. 2018;525:192–9.CrossRef
13.
go back to reference Nishizawa T, Sugimoto Y, Takeda T, Kodera Y, Hatano Y, Takahashi M, Okamoto H. Identification and whole genome characterization of novel anelloviruses in masked palm civets (Paguma larvata): Segregation into four distinct clades. Virus Res. 2018;256:183–91.CrossRef Nishizawa T, Sugimoto Y, Takeda T, Kodera Y, Hatano Y, Takahashi M, Okamoto H. Identification and whole genome characterization of novel anelloviruses in masked palm civets (Paguma larvata): Segregation into four distinct clades. Virus Res. 2018;256:183–91.CrossRef
14.
go back to reference Du J, Li YH, Lu L, Zheng DD, Liu B, Yang L, Su HX, Dong J, Sun LL, Zhu YF, et al. Biodiversity of rodent anelloviruses in China. Emerg Microb Infect. 2018;7:1–3. Du J, Li YH, Lu L, Zheng DD, Liu B, Yang L, Su HX, Dong J, Sun LL, Zhu YF, et al. Biodiversity of rodent anelloviruses in China. Emerg Microb Infect. 2018;7:1–3.
15.
go back to reference Cibulski SP, Teixeira TF, de Sales Lima FE, do Santos HF, Franco AC, Roehe PM. A novel Anelloviridae species detected in Tadarida brasiliensis bats: first sequence of a chiropteran Anellovirus. Genome Announce. 2014;2:e01028-14. Cibulski SP, Teixeira TF, de Sales Lima FE, do Santos HF, Franco AC, Roehe PM. A novel Anelloviridae species detected in Tadarida brasiliensis bats: first sequence of a chiropteran Anellovirus. Genome Announce. 2014;2:e01028-14.
16.
go back to reference Ng TFF, Suedmeyer WK, Wheeler E, Gulland F, Breitbartt M. Novel anellovirus discovered from a mortality event of captive California sea lions. J Gen Virol. 2009;90:1256–61.CrossRef Ng TFF, Suedmeyer WK, Wheeler E, Gulland F, Breitbartt M. Novel anellovirus discovered from a mortality event of captive California sea lions. J Gen Virol. 2009;90:1256–61.CrossRef
17.
go back to reference Ng TFF, Wheeler E, Greig D, Waltzek TB, Gulland F, Breitbart M. Metagenomic identification of a novel anellovirus in Pacific harbor seal (Phoca vitulina richardsii) lung samples and its detection in samples from multiple years. J Gen Virol. 2011;92:1318–23.CrossRef Ng TFF, Wheeler E, Greig D, Waltzek TB, Gulland F, Breitbart M. Metagenomic identification of a novel anellovirus in Pacific harbor seal (Phoca vitulina richardsii) lung samples and its detection in samples from multiple years. J Gen Virol. 2011;92:1318–23.CrossRef
18.
go back to reference Spandole S, Cimponeriu D, Berca LM, Mihaescu G. Human anelloviruses: an update of molecular, epidemiological and clinical aspects. Arch Virol. 2015;160:893–908.CrossRef Spandole S, Cimponeriu D, Berca LM, Mihaescu G. Human anelloviruses: an update of molecular, epidemiological and clinical aspects. Arch Virol. 2015;160:893–908.CrossRef
19.
go back to reference Pavlovic M, Chatterjee S, Kats A. Parvovirus b19 and auto antibodies reactive with ssDNA in lupus disease: bioinformatics analysis and hypothesis, Republic of Yemen. MOJ Immunol. 2018;6:281–6. Pavlovic M, Chatterjee S, Kats A. Parvovirus b19 and auto antibodies reactive with ssDNA in lupus disease: bioinformatics analysis and hypothesis, Republic of Yemen. MOJ Immunol. 2018;6:281–6.
20.
go back to reference Bernardin F, Operskalski E, Busch M, Delwart E. Transfusion transmission of highly prevalent commensal human viruses. Transfusion. 2010;50:2474–83.CrossRef Bernardin F, Operskalski E, Busch M, Delwart E. Transfusion transmission of highly prevalent commensal human viruses. Transfusion. 2010;50:2474–83.CrossRef
21.
go back to reference Phan TG, Kapusinszky B, Wang C, Rose RK, Lipton HL, Delwart EL. The fecal viral flora of wild rodents. PLoS Pathog. 2011;7:e1002218.CrossRef Phan TG, Kapusinszky B, Wang C, Rose RK, Lipton HL, Delwart EL. The fecal viral flora of wild rodents. PLoS Pathog. 2011;7:e1002218.CrossRef
22.
go back to reference Wekerle H, Kojima K, Lannes-Vieira J, Lassmann H, Linington C. Animal models. Ann Neurol. 1994;36:S47–53.CrossRef Wekerle H, Kojima K, Lannes-Vieira J, Lassmann H, Linington C. Animal models. Ann Neurol. 1994;36:S47–53.CrossRef
23.
go back to reference Zhang W, Yang SX, Shan TL, Hou R, Liu ZJ, Li W, Guo LH, Wang Y, Chen P, Wang XC, et al. Virome comparisons in wild-diseased and healthy captive giant pandas. Microbiome. 2017;5:90.CrossRef Zhang W, Yang SX, Shan TL, Hou R, Liu ZJ, Li W, Guo LH, Wang Y, Chen P, Wang XC, et al. Virome comparisons in wild-diseased and healthy captive giant pandas. Microbiome. 2017;5:90.CrossRef
24.
go back to reference Zhang W, Li LL, Deng XT, Blumel J, Nubling CM, Hunfeld A, Baylis SA, Delwart E. Viral nucleic acids in human plasma pools. Transfusion. 2016;56:2248–55.CrossRef Zhang W, Li LL, Deng XT, Blumel J, Nubling CM, Hunfeld A, Baylis SA, Delwart E. Viral nucleic acids in human plasma pools. Transfusion. 2016;56:2248–55.CrossRef
25.
go back to reference Yang J, Wang H, Zhang X, Yang S, Xu H, Zhang W. Viral metagenomic identification of a novel anellovirus in blood sample of a child with atopic dermatitis. J Med Virol. 2020;1–4. Yang J, Wang H, Zhang X, Yang S, Xu H, Zhang W. Viral metagenomic identification of a novel anellovirus in blood sample of a child with atopic dermatitis. J Med Virol. 2020;1–4.
26.
go back to reference Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402.CrossRef Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402.CrossRef
27.
go back to reference Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience. 2012;1:2047–217.CrossRef Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience. 2012;1:2047–217.CrossRef
28.
go back to reference Guo L, Hua X, Zhang W, Yang S, Shen Q, Hu H, Li J, Liu Z, Wang X, Wang H, et al. Viral metagenomics analysis of feces from coronary heart disease patients reveals the genetic diversity of the Microviridae. Virol Sin. 2017;32:130–8.CrossRef Guo L, Hua X, Zhang W, Yang S, Shen Q, Hu H, Li J, Liu Z, Wang X, Wang H, et al. Viral metagenomics analysis of feces from coronary heart disease patients reveals the genetic diversity of the Microviridae. Virol Sin. 2017;32:130–8.CrossRef
29.
go back to reference Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. MrBayes 32: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539–42.CrossRef Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. MrBayes 32: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539–42.CrossRef
30.
go back to reference De Vlaminck I, Khush KK, Strehl C, Kohli B, Luikart H, Neff NF, Okamoto J, Snyder TM, Cornfield DN, Nicolls MR. Temporal response of the human virome to immunosuppression and antiviral therapy. Cell. 2013;155:1178–87.CrossRef De Vlaminck I, Khush KK, Strehl C, Kohli B, Luikart H, Neff NF, Okamoto J, Snyder TM, Cornfield DN, Nicolls MR. Temporal response of the human virome to immunosuppression and antiviral therapy. Cell. 2013;155:1178–87.CrossRef
31.
go back to reference Eibach D, Hogan B, Sarpong N, Winter D, Struck NS, Adu-Sarkodie Y, Owusu-Dabo E, Schmidt-Chanasit J, May J, Cadar D. Viral metagenomics revealed novel betatorquevirus species in pediatric inpatients with encephalitis/meningoencephalitis from Ghana. Sci Rep. 2019;9:1–10.CrossRef Eibach D, Hogan B, Sarpong N, Winter D, Struck NS, Adu-Sarkodie Y, Owusu-Dabo E, Schmidt-Chanasit J, May J, Cadar D. Viral metagenomics revealed novel betatorquevirus species in pediatric inpatients with encephalitis/meningoencephalitis from Ghana. Sci Rep. 2019;9:1–10.CrossRef
32.
go back to reference Walker PJ, Siddell SG, Lefkowitz EJ, Mushegian AR, Adriaenssens EM, Dempsey DM, Dutilh BE, Harrach B, Harrison RL, Hendrickson RC, et al. Changes to virus taxonomy and the Statutes ratified by the International Committee on Taxonomy of Viruses (2020). Arch Virol. 2020;165:2737–48.CrossRef Walker PJ, Siddell SG, Lefkowitz EJ, Mushegian AR, Adriaenssens EM, Dempsey DM, Dutilh BE, Harrach B, Harrison RL, Hendrickson RC, et al. Changes to virus taxonomy and the Statutes ratified by the International Committee on Taxonomy of Viruses (2020). Arch Virol. 2020;165:2737–48.CrossRef
33.
go back to reference Biagini P, Bendinelli M, Hino S, Kakkola L, Mankertz A, Niel C, Okamoto H, Raidal S, Teo C, Todd D. Family Anelloviridae. In: Virus taxonomy: Ninth report of the international committee on taxonomy of viruses. Elsevier Scientific Publ. Co; 2011. p. 331–341. Biagini P, Bendinelli M, Hino S, Kakkola L, Mankertz A, Niel C, Okamoto H, Raidal S, Teo C, Todd D. Family Anelloviridae. In: Virus taxonomy: Ninth report of the international committee on taxonomy of viruses. Elsevier Scientific Publ. Co; 2011. p. 331–341.
34.
go back to reference Hameed M, Liu K, Anwar MN, Wahaab A, Li C, Di D, Wang X, Khan S, Xu J, Li B. A viral metagenomic analysis reveals rich viral abundance and diversity in mosquitoes from pig farms. Transbound Emerg Dis. 2020;67:328–43.CrossRef Hameed M, Liu K, Anwar MN, Wahaab A, Li C, Di D, Wang X, Khan S, Xu J, Li B. A viral metagenomic analysis reveals rich viral abundance and diversity in mosquitoes from pig farms. Transbound Emerg Dis. 2020;67:328–43.CrossRef
35.
go back to reference Wei J, Hameed M, Wahaab A, Shan T, Wang X, Khan S, Di D, Xiqian L, Zhang J-J, Anwar MN. A metagenomic analysis of mosquito virome collected from different animal farms at Yunnan-Myanmar border of China. Front Microbiol. 2020;11:3601. Wei J, Hameed M, Wahaab A, Shan T, Wang X, Khan S, Di D, Xiqian L, Zhang J-J, Anwar MN. A metagenomic analysis of mosquito virome collected from different animal farms at Yunnan-Myanmar border of China. Front Microbiol. 2020;11:3601.
36.
go back to reference Davidson I, Shulman L. Unraveling the puzzle of human anellovirus infections by comparison with avian infections with the chicken anemia virus. Virus Res. 2008;137:1–15.CrossRef Davidson I, Shulman L. Unraveling the puzzle of human anellovirus infections by comparison with avian infections with the chicken anemia virus. Virus Res. 2008;137:1–15.CrossRef
Metadata
Title
Viral metagenomics reveals two novel anelloviruses in feces of experimental rats
Authors
Song-Yi Ning
Ming-Ming Zhou
Jie Yang
Jian Zeng
Jia-Ping Wang
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2021
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-021-01723-9

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