Skip to main content

Advertisement

Log in

Detection of bat-associated circoviruses in Korean bats

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

In recent years, several novel circular single-stranded DNA viruses have been detected in various mammals, birds, insects, and environmental samples using metagenomic and high-throughput sequencing approaches. In this study, we tested for the presence of circoviruses in 243 bat fecal samples collected between 2018 and 2019 from 48 sampling sites across Korea. To detect circoviruses, nested PCR was performed with degenerate primers targeting a conserved replication-associated protein (rep) gene of circovirus/cyclovirus. Among 243 samples tested, a total of 37 fecal samples from 14 sampling sites were PCR-positive for circoviruses at a frequency rate of 15.23%. We obtained 36 partial rep gene sequences of circoviruses and one complete genome sequence of bat-associated circovirus 12, encompassing a genome size of 2097 nt containing two inversely arranged open reading frames and a conserved nonamer sequence in the apex of a stem-loop structure. In addition, we found four bat species that were harboring circoviruses in Korea based on species identification PCR of circovirus-positive bat fecal samples. Detailed sequence analysis indicated that the bat-associated circovirus sequences identified in this study were related to those of known bat and avian groups of circoviruses. Herein, we report evidence for the presence of bat-associated circoviruses in Korean bats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Availability of data and material

The data presented in this article are openly available in the GenBank database at https://www.ncbi.nlm.nih.gov/genbank/, reference number [MW506294-MW506329, MW732037].

References

  1. Rosario K, Breitbart M, Harrach B, Segalés J, Delwart E, Biagini P, Varsani A (2017) Revisiting the taxonomy of the family Circoviridae: establishment of the genus Cyclovirus and removal of the genus Gyrovirus. Arch Virol 162:1447–1463. https://doi.org/10.1007/s00705-017-3247-y

    Article  CAS  PubMed  Google Scholar 

  2. Hamel AL, Lin LL, Nayar GP (1998) Nucleotide sequence of porcine circovirus associated with postweaning multisystemic wasting syndrome in pigs. J Virol 72:5262–5267. https://doi.org/10.1128/JVI.72.6.5262-5267.1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Palinski R, Piñeyro P, Shang P, Yuan F, Guo R, Fang Y, Byers E, Hause BM (2016) A novel porcine circovirus distantly related to known circoviruses is associated with porcine dermatitis and nephropathy syndrome and reproductive failure. J Virol 91:e01879-e1916. https://doi.org/10.1128/JVI.01879-16

    Article  PubMed  PubMed Central  Google Scholar 

  4. Latimer KS, Rakich PM, Steffens WL, Kircher IM, Ritchie BW, Niagro FD, Lukert PD (1991) A novel DNA virus associated with feather inclusions in psittacine beak and feather disease. Vet Pathol 28:300–304. https://doi.org/10.1177/030098589102800406

    Article  CAS  PubMed  Google Scholar 

  5. Raue R, Schmidt V, Freick M, Reinhardt B, Johne R, Kamphausen L, Kaleta EF, Müller H, Krautwald-Junghanns ME (2005) A disease complex associated with pigeon circovirus infection, young pigeon disease syndrome. Avian Pathol 34:418–425. https://doi.org/10.1080/03079450500267825

    Article  PubMed  Google Scholar 

  6. Stenzel T, Koncicki A (2017) The epidemiology, molecular characterization and clinical pathology of circovirus infections in pigeons—current knowledge. Vet Q 37:166–174. https://doi.org/10.1080/01652176.2017.1325972

    Article  PubMed  Google Scholar 

  7. Lian H, Liu Y, Li N, Wang Y, Zhang S, Hu R (2014) Novel circovirus from mink, China. Emerg Infect Dis 20:1548–1550. https://doi.org/10.3201/eid2009.140015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Li L, McGraw S, Zhu K, Leutenegger CM, Marks SL, Kubiski S, Gaffney P, Dela-Cruz FN Jr, Wang C, Delwart E, Pesavento PA (2013) Circovirus in tissues of dogs with vasculitis and hemorrhage. Emerg Infect Dis 19:534–541. https://doi.org/10.3201/eid1904.121390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Todd D (2000) Circoviruses: immunosuppressive threats to avian species: a review. Avian Pathol 29:373–394. https://doi.org/10.1080/030794500750047126

    Article  CAS  PubMed  Google Scholar 

  10. Shulman LM, Davidson I (2017) Viruses with circular single-stranded DNA genomes are everywhere! Annu Rev Virol 4:159–180. https://doi.org/10.1146/annurev-virology-101416-041953

    Article  CAS  PubMed  Google Scholar 

  11. Lőrincz M, Cságola A, Farkas SL, Székely C, Tuboly T (2011) First detection and analysis of a fish circovirus. J Gen Virol 92:1817–1821. https://doi.org/10.1099/vir.0.031344-0

    Article  CAS  PubMed  Google Scholar 

  12. Lőrincz M, Dán A, Láng M, Csaba G, Tóth AG, Székely C, Cságola A, Tuboly T (2012) Novel circovirus in European catfish (Silurus glanis). Arch Virol 157:1173–1176. https://doi.org/10.1007/s00705-012-1291-1

    Article  CAS  PubMed  Google Scholar 

  13. Fisher M, Harrison T, Nebroski M, Kruczkiewicz P, Rothenburger JL, Ambagala A, Macbeth B, Lung O (2020) Discovery and comparative genomic analysis of elk circovirus (ElkCV), a novel circovirus species and the first reported from a cervid host. Sci Rep 10:19548. https://doi.org/10.1038/s41598-020-75577-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Johne R, Fernández-de-Luco D, Höfle U, Müller H (2006) Genome of a novel circovirus of starlings, amplified by multiply primed rolling-circle amplification. J Gen Virol 87:1189–1195. https://doi.org/10.1099/vir.0.81561-0

    Article  CAS  PubMed  Google Scholar 

  15. Todd D, Weston J, Ball NW, Borghmans BJ, Smyth JA, Gelmini L, Lavazza A (2001) Nucleotide sequence-based identification of a novel circovirus of canaries. Avian Pathol 30:321–325. https://doi.org/10.1080/03079450120066322

    Article  CAS  PubMed  Google Scholar 

  16. Blinkova O, Rosario K, Li L, Kapoor A, Slikas B, Bernardin F, Breitbart M, Delwart E (2009) Frequent detection of highly diverse variants of cardiovirus, cosavirus, bocavirus, and circovirus in sewage samples collected in the United States. J Clin Microbiol 47:3507–3513. https://doi.org/10.1128/JCM.01062-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Rosario K, Duffy S, Breitbart M (2009) Diverse circovirus-like genome architectures revealed by environmental metagenomics. J Gen Virol 90:2418–2424. https://doi.org/10.1099/vir.0.012955-0

    Article  CAS  PubMed  Google Scholar 

  18. Brook CE, Dobson AP (2015) Bats as “special” reservoirs for emerging zoonotic pathogens. Trends Microbiol 23:172–180. https://doi.org/10.1016/j.tim.2014.12.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Ge X, Li J, Peng C, Wu L, Yang X, Wu Y, Zhang Y, Shi Z (2011) Genetic diversity of novel circular ssDNA viruses in bats in China. J Gen Virol 92:2646–2653. https://doi.org/10.1099/vir.0.034108-0

    Article  CAS  PubMed  Google Scholar 

  20. Lima FE, Cibulski SP, Dos Santos HF, Teixeira TF, Varela AP, Roehe PM, Delwart E, Franco AC (2015) Genomic characterization of novel circular ssDNA viruses from insectivorous bats in Southern Brazil. PLoS ONE 10:e0118070. https://doi.org/10.1371/journal.pone.0118070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wu Z, Yang L, Ren X, He G, Zhang J, Yang J, Qian Z, Dong J, Sun L, Zhu Y, Du J, Yang F, Zhang S, Jin Q (2016) Deciphering the bat virome catalog to better understand the ecological diversity of bat viruses and the bat origin of emerging infectious diseases. ISME J 10:609–620. https://doi.org/10.1038/ismej.2015.138

    Article  PubMed  Google Scholar 

  22. Matsumoto T, Sato M, Nishizono A, Ahmed K (2019) A novel bat-associated circovirus identified in northern Hokkaido, Japan. Arch Virol 164:2179–2182. https://doi.org/10.1007/s00705-019-04286-x

    Article  CAS  PubMed  Google Scholar 

  23. He B, Li Z, Yang F, Zheng J, Feng Y, Guo H, Li Y, Wang Y, Su N, Zhang F, Fan Q, Tu C (2013) Virome profiling of bats from Myanmar by metagenomic analysis of tissue samples reveals more novel Mammalian viruses. PLoS ONE 8:e61950. https://doi.org/10.1371/journal.pone.0061950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Li L, Kapoor A, Slikas B, Bamidele OS, Wang C, Shaukat S, Masroor MA, Wilson ML, Ndjango JB, Peeters M, Gross-Camp ND, Muller MN, Hahn BH, Wolfe ND, Triki H, Bartkus J, Zaidi SZ, Delwart E (2010) Multiple diverse circoviruses infect farm animals and are commonly found in human and chimpanzee feces. J Virol 84:1674–1682. https://doi.org/10.1128/JVI.02109-09

    Article  CAS  PubMed  Google Scholar 

  25. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Window 95/98/NT. Nucleic Acids Symp 41:95–98

    CAS  Google Scholar 

  26. Schlegel M, Ali HS, Stieger N, Groschup MH, Wolf R, Ulrich RG (2012) Molecular identification of small mammal species using novel cytochrome B gene-derived degenerated primers. Biochem Genet 50:440–447. https://doi.org/10.1007/s10528-011-9487-8

    Article  CAS  PubMed  Google Scholar 

  27. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023

    Article  CAS  PubMed  Google Scholar 

  29. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282. https://doi.org/10.1093/bioinformatics/8.3.275

    Article  CAS  PubMed  Google Scholar 

  30. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Stenzel T, Farkas K, Varsani A (2015) Genome sequence of a diverse goose circovirus recovered from greylag goose. Genome Announc 3:e00767-e815. https://doi.org/10.1128/genomeA.00767-15

    Article  PubMed  PubMed Central  Google Scholar 

  32. Todd D, Weston JH, Soike D, Smyth JA (2001) Genome sequence determinations and analyses of novel circoviruses from goose and pigeon. Virology 286:354–362. https://doi.org/10.1006/viro.2001.0985

    Article  CAS  PubMed  Google Scholar 

  33. Loiko MR, Junqueira DM, Varela A, Tochetto C, Scheffer CM, Lima DA, Morel AP, Cerva C, Paim WP, Mayer FQ, Roehe PM (2018) Columbid circoviruses detected in free ranging pigeons from Southern Brazil: insights on PiCV evolution. Arch Virol 163:3083–3090. https://doi.org/10.1007/s00705-018-3990-8

    Article  CAS  PubMed  Google Scholar 

  34. Cheung AK (2006) Rolling-circle replication of an animal circovirus genome in a theta-replicating bacterial plasmid in Escherichia coli. J Virol 80:8686–8694. https://doi.org/10.1128/JVI.00655-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Han HJ, Wen HL, Zhao L, Liu JW, Luo LM, Zhou CM, Qin XR, Zhu YL, Liu MM, Qi R, Li WQ, Yu H, Yu XJ (2017) Novel coronaviruses, astroviruses, adenoviruses and circoviruses in insectivorous bats from northern China. Zoonoses Public Health 64:636–646. https://doi.org/10.1111/zph.12358

    Article  CAS  PubMed  Google Scholar 

  36. Han S, Jung CW, Choi YG, Kim SS (2012) Sounds of the bats in Korea. National Institute of Biological Resources Press, Incheon

    Google Scholar 

  37. Xie J, Li Y, Shen X, Goh G, Zhu Y, Cui J, Wang LF, Shi ZL, Zhou P (2018) Dampened STING-dependent interferon activation in bats. Cell Host Microbe 23:297–301. https://doi.org/10.1016/j.chom.2018.01.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Breitbart M, Delwart E, Rosario K, Segalés J, Varsani A, ICTV Report Consortium (2017) ICTV virus taxonomy profile: circoviridae. J Gen Virol 98:1997–1998. https://doi.org/10.1099/jgv.0.000871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Lecis R, Mucedda M, Pidinchedda E, Zobba R, Pittau M, Alberti A (2020) Genomic characterization of a novel bat-associated circovirus detected in European Miniopterus schreibersii bats. Virus Genes 56:325–328. https://doi.org/10.1007/s11262-020-01747-3

    Article  CAS  PubMed  Google Scholar 

  40. Martin DP, Biagini P, Lefeuvre P, Golden M, Roumagnac P, Varsani A (2011) Recombination in eukaryotic single stranded DNA viruses. Viruses 3:1699–1738. https://doi.org/10.3390/v3091699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Li L, Shan T, Soji OB, Alam MM, Kunz TH, Zaidi SZ, Delwart E (2011) Possible cross-species transmission of circoviruses and cycloviruses among farm animals. J Gen Virol 92:768–772. https://doi.org/10.1099/vir.0.028704-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Li L, Victoria JG, Wang C, Jones M, Fellers GM, Kunz TH, Delwart E (2010) Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. J Virol 84:6955–6965. https://doi.org/10.1128/JVI.00501-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Wang LF, Anderson DE (2019) Viruses in bats and potential spillover to animals and humans. Curr Opin Virol 347:9–89. https://doi.org/10.1016/j.coviro.2018.12.007

    Article  Google Scholar 

  44. 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

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by KRIBB and the Bio Nano Health-Guard Research Center, funded by the Ministry of Science and ICT (MSIT) of Korea, as a Global Frontier Project (grant no. H-GUARD_2013M3A6B2078954) and by the Young Researcher Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Science and ICT of Korea (NRF-2020R1C1C1010440). This work was also supported by "Regional Innovation Strategy (RIS)" through the National Research Foundation of Korea (NRF), funded by the Ministry of Education (MOE).

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: GD, SWY, DGJ. Methodology: GD, JYN, SSJ. Formal analysis and investigation: GD, SWY. Writing—original draft preparation: GD. Writing—review and editing: HKK, DGJ. Funding acquisition: HKK, DGJ. Resources: YGC. Supervision: HKK, DGJ.

Corresponding authors

Correspondence to Dae Gwin Jeong or Hye Kwon Kim.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Ethical approval

To avoid animal disturbance, this study used dropped guano from beneath bat roosting sites/colonies in Korea without capturing or interfering with the roosting bats. Additionally, the bat guano was collected by an expert from the Korean Institute of Biospeleology during the cave investigation period. This sampling design did not require ethical approval for the study, and therefore, none was obtained. The authors confirm that the ethical policies of the journal, as noted on the journal’s author guidelines page, have been adhered to.

Additional information

Handling Editor: Akbar Dastjerdi.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (TXT 18 KB)

Supplementary file2 (XLSX 30 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dhandapani, G., Yoon, SW., Noh, J.Y. et al. Detection of bat-associated circoviruses in Korean bats. Arch Virol 166, 3013–3021 (2021). https://doi.org/10.1007/s00705-021-05202-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-021-05202-y