Advertisement

Archives of Virology

, Volume 164, Issue 4, pp 1015–1025 | Cite as

Detection of adenovirus, papillomavirus and parvovirus in Brazilian bats of the species Artibeus lituratus and Sturnira lilium

  • Fernando FinokettiEmail author
  • Raíssa Nunes dos Santos
  • Aline Alves Scarpellini Campos
  • André Luís da Silva Zani
  • Camila Mosca Barboza
  • Marcélia Emanuele Sad Fernandes
  • Tatiane de Cassia Pardo de Souza
  • Driele Delanira dos Santos
  • Giovana Werneck Bortolanza
  • Henrique Ortêncio Filho
  • Paulo Michel Roehe
  • Ana Cláudia Franco
  • Helena Beatriz de Carvalho Ruthner Batista
Original Article

Abstract

Bats play a significant role in maintaining their ecosystems through pollination, dispersal of seeds, and control of insect populations, but they are also known to host many microorganisms and have been described as natural reservoirs for viruses with zoonotic potential. The diversity of viruses in these animals remains largely unknown, however, because studies are limited by species, location, virus target, or sample type. Therefore, the aim of this study was to detect fragments of viral genomes in bat samples. We performed high-throughput sequencing analysis and specific PCR and RT-PCR on pools of anal and oropharyngeal swabs from Artibeus lituratus and Sturnira lilium collected in southern Brazil. As a result, a member of the family Adenoviridae related to human adenovirus C was detected in anal swabs from S. lilium. In addition, we detected a papillomavirus in an anal swab from A. lituratus. Our analyses also allowed the detection of adenoviruses and parvoviruses in oropharyngeal swabs collected from A. lituratus. These results increase our knowledge about viral diversity and illustrate the importance of conducting virus surveillance in bats.

Notes

Acknowledgements

We thank Dra. Fabiana Quoos Mayer from Instituto de Pesquisas Veterinárias Desidério Finamor. All authors have seen and approved the manuscript and have contributed significantly to the work.

Funding

This study was supported by a grant from FAPESP, Brazil, in 2016 (Project Code No. 2015/25367-0) and the Secretary of State for Health of São Paulo. Part of this work was supported by CNPq and CAPES. A. C. F. and P. M. R. are CNPq fellows.

Compliance with ethical standards

Conflict of interest

All authors declare that there are no financial or other relationships that might lead to a conflict of interest.

References

  1. 1.
    Allocati N, Petrucci AG, Di Giovanni P, Masulli M, Di Ilio C, De Laurenzi V (2016) Bat–man disease transmission: zoonotic pathogens from wildlife reservoirs to human populations. Cell Death Discov.  https://doi.org/10.1038/cddiscovery.2016.48 Google Scholar
  2. 2.
    Serra-Cobo J, López-Roig M (2016) Bats and emerging infections: an ecological and virological puzzle. Adv Exp Med Biol.  https://doi.org/10.1007/5584_2016_131 Google Scholar
  3. 3.
    Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, Wong BH, Wong SS, Leung SY, Chan KH, Yuen KY (2005) Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci USA 102:14040–14045.  https://doi.org/10.1073/pnas.0506735102 CrossRefGoogle Scholar
  4. 4.
    Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H, Zhang J, McEachern J, Field H, Daszak P, Eaton BT, Zhang S, Wang LF (2005) Bats are natural reservoirs of SARS-like coronaviruses. Science 310:676–679.  https://doi.org/10.1126/science.1118391 CrossRefGoogle Scholar
  5. 5.
    Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, Yaba P, Délicat A, Paweska JT, Gonzalez JP, Swanepoel R (2005) Fruit bats as reservoirs of Ebola virus. Nature 438:557–575.  https://doi.org/10.1038/438575a CrossRefGoogle Scholar
  6. 6.
    Guo WP, Lin XD, Wang W, Tian JH, Cong ML, Zhang HL, Wang MR, Zhou RH, Wang JB, Li MH, Xu J, Holmes EC, Zhang YZ (2013) Phylogeny and origins of hantaviruses harbored by bats, insectivores, and rodents. PLoS Pathog 9:e1003159.  https://doi.org/10.1371/journal.ppat.1003159 CrossRefGoogle Scholar
  7. 7.
    Halpin K, Hyatt AD, Fogarty R, Middleton D, Bingham J, Epstein JH, Rahman SA, Hughes T, Smith C, Field HE, Daszak P, Henipavirus Ecology Research Group (2011) Pteropid bats are confirmed as the reservoir hosts of henipaviruses: a comprehensive experimental study of virus transmission. Am J Trop Med Hyg 85:946–951.  https://doi.org/10.4269/ajtmh.2011.10-0567 CrossRefGoogle Scholar
  8. 8.
    Smith I, Wang LF (2013) Bats and their virome: an important source of emerging viruses capable of infecting humans. Curr Opin Virol 3:84–91.  https://doi.org/10.1016/j.coviro.2012.11.006 CrossRefGoogle Scholar
  9. 9.
    Geoghegan JL, Duchêne S, Holmes EC (2017) Comparative analysis estimates the relative frequencies of co-divergence and cross-species transmission within viral families. PLoS Pathog 13(2):e1006215.  https://doi.org/10.1371/journal.ppat.1006215 CrossRefGoogle Scholar
  10. 10.
    Hackenbrack N, Rogers MB, Ashley RE, Keel MK, Kubiski SV, Bryan JA, Ghedin E, Holmes EC, Hafenstein SL, Allison AB (2017) Evolution and cryo-electron microscopy capsid structure of a North American bat adenovirus and its relationship to other mastadenoviruses. J Virol 91:e01504–e01516.  https://doi.org/10.1128/JVI.01504-16 CrossRefGoogle Scholar
  11. 11.
    Li Y, Ge X, Zhang H, Zhou P, Zhu Y, Zhang Y, Yuan J, Wang LF, Shi Z (2010) Host range, prevalence, and genetic diversity of adenoviruses in bats. J Virol 84:3889–3897.  https://doi.org/10.1128/JVI.02497-09 CrossRefGoogle Scholar
  12. 12.
    Kohl C, Vidovszky MZ, Mühldorfer K, Dabrowski PW, Radonic A, Nitsche A, Wibbelt G, Kurth A, Harrach B (2012) Genome analysis of bat adenovirus 2: indications of interspecies transmission. J Virol 86:1888–1892.  https://doi.org/10.1128/JVI.05974-11 CrossRefGoogle Scholar
  13. 13.
    Tan B, Yang XL, Ge XY, Peng C, Zhang YZ, Zhang LB, Shi ZL (2016) Novel bat adenoviruses with an extremely large E3 gene. J Gen Virol 97:1625–1635.  https://doi.org/10.1099/jgv.0.000470 CrossRefGoogle Scholar
  14. 14.
    Tan B, Yang XL, Ge XY, Peng C, Liu HZ, Zhang YZ, Zhang LB, Shi ZL (2017) Novel bat adenoviruses with low G+C content shed new light on the evolution of adenoviruses. J Gen Virol 98:739–748.  https://doi.org/10.1099/jgv.0.000739 CrossRefGoogle Scholar
  15. 15.
    Ogawa H, Kajihara M, Nao N, Shigeno A, Fujikura D, Hang’Ombe BM, Mweene AS, Mutemwa A, Squarre D, Yamada M, Higashi H, Sawa H, Takada A (2017) Characterization of a novel bat adenovirus isolated from straw-colored fruit bat (Eidolon helvum). Viruses 9(12):1–16.  https://doi.org/10.3390/v9120371 CrossRefGoogle Scholar
  16. 16.
    Lima FES, Cibulski SP, Elesbao F, JrP Carnieli, Batista HBCR, Roehe PM, Franco AC (2013) First detection of adenovirus in the vampire bat (Desmodus rotundus) in Brazil. Virus Genes.  https://doi.org/10.1007/s11262-013-0947-6 Google Scholar
  17. 17.
    García-Pérez R, Ibáñez C, Godínez JM, Aréchiga N, Garin I, Pérez-Suárez G, de Paz O, Juste J, Echevarría JE, Bravo IG (2014) Novel papillomaviruses in free-ranging iberian bats: no virus–host co-evolution, no Strict host specificity, and hints for recombination. Genome Biol Evol 6(1):94–104.  https://doi.org/10.1093/gbe/evt211 CrossRefGoogle Scholar
  18. 18.
    Hu D, Zhu C, Wang Y, Ai L, Yang L, Ye F, Ding C, Chen J, He B, Zhu J, Qian H, Xu W, Feng Y, Tan W, Wang C (2017) Virome analysis for identification of novel mammalian viruses in bats from Southeast China. Sci Rep 7(1):10917.  https://doi.org/10.1038/s41598-017-11384-w CrossRefGoogle Scholar
  19. 19.
    Salmier A, Tirera S, de Thoisy B, Franc A, Darcissac E, Donato D, Bouchier C, Lacoste V, Lavergne A (2017) Virome analysis of two sympatric bat species (Desmodus rotundus and Molossus molossus) in French Guiana. PLoS One 12(11):e0186943.  https://doi.org/10.1371/journal.pone.0186943 CrossRefGoogle Scholar
  20. 20.
    de Souza WM, Romeiro MF, Fumagalli MJ, Modha S, de Araujo J, Queiroz LH, Durigon EL, Figueiredo LTM, Murcia PR, Gifford RJ (2017) Chapparvoviruses occur in at least three vertebrate classesand have a broad biogeographic distribution. J Gen Virol 98:225–229.  https://doi.org/10.1099/jgv.0.000671 CrossRefGoogle Scholar
  21. 21.
    Kemenesi G, Dallos B, Görföl T, Estók P, Boldogh S, Kurucz K, Oldal M, Marton S, Bányai K, Jakab F (2015) Genetic diversity and recombination within bufaviruses: detection of a novel strain in Hungarian bats. Infect Genet Evol.  https://doi.org/10.1016/j.meegid.2015.05.017 Google Scholar
  22. 22.
    Lau SKP, Ahmed SS, Yeung HC, Li KS, Fan RY, Cheng TY, Cai JP, Wang M, Zheng BJ, Wong SS, Woo PC, Yuen KY (2016) Identification and interspecies transmission of a novel bocaparvovirus among different bat species in China. J Gen Virol 97:3345–3358.  https://doi.org/10.1099/jgv.0.000645 CrossRefGoogle Scholar
  23. 23.
    Sasaki M, Gonzalez G, Wada Y, Setiyono A, Handharyani E, Rahmadani I, Taha S, Adiani S, Latief M, Kholilullah ZA, Subangkit M, Kobayashi S, Nakamura I, Kimura T, Orba Y, Ito K, Sawa H (2016) Divergent bufavirus harboured in megabats represents a new lineage of parvoviruses. Sci Rep 6:24257.  https://doi.org/10.1038/srep24257 CrossRefGoogle Scholar
  24. 24.
    Moratelli R, Calisher CH (2015) Bats and zoonotic viruses: can we confidently link bats with emerging deadly viruses? Mem Inst Oswaldo Cruz 10(1):1–22.  https://doi.org/10.1590/0074-02760150048 CrossRefGoogle Scholar
  25. 25.
    Baker KS, Leggett RM, Bexfield NH, Alston M, Daly G, Todd S, Tachedjian M, Holmes CE, Crameri S, Wang LF, Heeney JL, Suu-Ire R, Kellam P, Cunningham AA, Wood JL, Caccamo M, Murcia PR (2013) Metagenomic study of the viruses of African straw-coloured fruit bats: detection of a chiropteran poxvirus and isolation of a novel adenovirus. Virology 441(2):95–106.  https://doi.org/10.1016/j.virol.2013.03.014 CrossRefGoogle Scholar
  26. 26.
    Male MF, Kraberger S, Stainton D, Kami V, Varsani A (2016) Cycloviruses, gemycircularviruses and other novel replication-associated protein encoding circular viruses in Pacific flying fox (Pteropus tonganus) faeces. Infect Genet Evol 39:279–292.  https://doi.org/10.1016/j.meegid.2016.02.009 CrossRefGoogle Scholar
  27. 27.
    Cibulski SP, Teixeira TF, Lima FES, do Santos HF, Franco AC, Roehe PM (2014) A novel Anelloviridae species detected in Tadarida brasiliensis bats: first sequence of a chiropteran Anellovirus. Genome Announc 2(5):e01028-14.  https://doi.org/10.1128/genomea.01028-14 CrossRefGoogle Scholar
  28. 28.
    Lima FES, Cibulski SP, Witt AA, Franco AC, Roehe PM (2015) Genomic characterization of two novel polyomaviruses in Brazilian insectivorous bats. Arch Virol.  https://doi.org/10.1007/s00705-015-2447-6 Google Scholar
  29. 29.
    Asano KM, Hora AS, Scheffer KC, Fahl WO, Iamamoto K, Mori E, Brandão PE (2016) Alphacoronavirus in urban Molossidae and Phyllostomidae bats, Brazil. Virol J 24(13):110.  https://doi.org/10.1186/s12985-016-0569-4 CrossRefGoogle Scholar
  30. 30.
    Góes LGB, Campos ACA, de Carvalho C, Ambar G, Queiroz LH, Cruz-Neto AP, Munir M, Durigon EL (2016) Genetic diversity of bats coronaviruses in the Atlantic Forest hotspot biome, Brazil. Infect Genet Evol 44:510–513.  https://doi.org/10.1016/j.meegid.2016.07.034 CrossRefGoogle Scholar
  31. 31.
    Greenhall GG, Paradiso JL (1968) BaLs and hal handing. Washington, U.S. Dep. In: Fish and wildlife service. Bureau 01’ Sport Fisheries and Wildlife, p 45Google Scholar
  32. 32.
    Straube FC, Bianconi GV (2002) Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes-de-neblina. Chiroptera Neotropical Brasília 8(1–2):150–152Google Scholar
  33. 33.
    Vizotto LD, Taddei VA (1973) Chave para determinação de quirópteros brasileiros. São José do Rio Preto, Gráfica Francal, p 72pGoogle Scholar
  34. 34.
    Jones JK, Carter DC (1976) Annotated checklist, with keys to subfamilies and genera. In: Baber RJ, Jones Jr., JK, Carter DC (eds) Biology of bats of the new world family Phyllostomidae, part I. Lubbock: Museum Texas Tech. University, pp 7–38 (Special Publications) Google Scholar
  35. 35.
    Gregorin R, Taddei VA (2002) Chave artificial para identificação de molossídeos brasileiros (Mammalia, Chiroptera). Mastozoologia Neotropical 1(9):13–32Google Scholar
  36. 36.
    Kluge M, Campos FS, Tavares M, de Amorim DB, Valdez FP, Giongo A, Roehe PM, Franco AC (2016) Metagenomic survey of viral diversity obtained from feces of subantarctic and south american fur seals. PLoS One 11(3):e0151921.  https://doi.org/10.1371/journal.pone.0151921 CrossRefGoogle Scholar
  37. 37.
    Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  38. 38.
    Stang A, Korn K, Wildner O, Uberla K (2005) Characterization of virus isolates by particle-associated nucleic acid PCR. J Clin Microbiol 43:716–720.  https://doi.org/10.1128/JCM.43.2.716-720.2005 CrossRefGoogle Scholar
  39. 39.
    JrP Carnieli, Brandão PE, Carrieri ML, Castilho JG, Macedo CI, Machado LM, Rangel N, de Carvalho RC, de Carvalho VA, Montebello L, Wada M, Kotait I (2006) Molecular epidemiology of rabies virus strains isolated from wild canids in Northeastern Brazil. Virus Res 120(1–2):113–120.  https://doi.org/10.1016/j.virusres.2006.02.007 Google Scholar
  40. 40.
    Razafindratsimandresy R, Jeanmaire EM, Counor D, Vasconcelos PF, Sall AA, Reynes JM (2009) Partial molecular characterization of alphaherpesviruses isolated from tropical bats. J Gen Virol 90(Pt 1):44–47.  https://doi.org/10.1099/vir.0.006825-0 CrossRefGoogle Scholar
  41. 41.
    Tong S, Chern SW, Li Y, Pallansch MA, Anderson LJ (2008) Sensitive and broadly reactive reverse transcription-PCR assays to detect novel paramyxoviruses. J Clin Microbiol 46(8):2652–2658.  https://doi.org/10.1128/JCM.00192-08 CrossRefGoogle Scholar
  42. 42.
    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(4):e61950.  https://doi.org/10.1371/journal.pone.0061950 CrossRefGoogle Scholar
  43. 43.
    Wang J, Moore NE, Murray ZL, McInnes K, White DJ, Tompkins DM, Hall RJ (2015) Discovery of novel virus sequences in an isolated and threatened bat species, the New Zealand lesser short-tailed bat (Mystacina tuberculata). J Gen Virol 96:2442–2452.  https://doi.org/10.1099/vir.0.000158 CrossRefGoogle Scholar
  44. 44.
    Yinda CK, Conceição-Neto N, Zeller M, Heylen E, Maes P, Ghogomu SM, Ranst MV, Matthijnssens J (2017) Novel highly divergent sapoviruses detected by metagenomics analysis in straw-colored fruit bats in Cameroon. Emerg Microbes Infect.  https://doi.org/10.1038/emi.2017.20 Google Scholar
  45. 45.
    Bibby K, Peccia J (2013) Identification of viral pathogen diversity in sewage sludge by metagenome analysis. Environ Sci Technol 47(4):1945–1951.  https://doi.org/10.1021/es305181x CrossRefGoogle Scholar
  46. 46.
    Staggemeier R, Heck TM, Demoliner M, Ritzel RG, Röhnelt NM, Girardi V, Venker CA, Spilki FR (2017) Enteric viruses and adenovirus diversity in waters from 2016 Olympic venues. Sci Total Environ 586:304–312.  https://doi.org/10.1016/j.scitotenv.2017.01.223 CrossRefGoogle Scholar
  47. 47.
    Jiang SC (2006) Human adenoviruses in water: occurrence and health implications: a critical review. Environ Sci Technol 40(23):7132–7140CrossRefGoogle Scholar
  48. 48.
    Barardi CRM, Viancelli A, Rigotto C, Correa AA, Moresco V, Souza DSM, ElMahdy MEI, Fongaro G, Pilotto MR, Nascimento MA (2012) Monitoring viruses in environmental samples. Intern J Environ Sci Eng 3:62–67Google Scholar
  49. 49.
    Chen EC, Yagi S, Kelly KR, Mendoza SP, Maninger N, Rosenthal A, Spinner A, Bales KL, Schnurr DP, Lerche NW, Chiu CY (2011) Cross-species transmission of a novel adenovirus associated with a fulminant pneumonia outbreak in a new world monkey colony. PLoS Pathog 7(7):e1002155.  https://doi.org/10.1371/journal.ppat.1002155 CrossRefGoogle Scholar
  50. 50.
    Tse H, Tsang AKL, Tsoi HW, Leung ASP, Ho CC, Lau SKP, Woo PCY, Yuen KY (2012) Identification of a novel bat papillomavirus by metagenomics. PLoS One 7(8):e43986.  https://doi.org/10.1371/journal.pone.0043986 CrossRefGoogle Scholar
  51. 51.
    Wu Z, Ren X, Yang L, Hu Y, Yang J, He G, Zhang J, Dong J, Sun L, Du J, Liu L, Xue Y, Wang J, Yang F, Zhang S, Jin Q (2012) Virome analysis for identification of novel mammalian viruses in bat species from Chinese provinces. J Virol 86(20):10999–11012.  https://doi.org/10.1128/JVI.01394-12 CrossRefGoogle Scholar
  52. 52.
    Rector A, Mostmans S, Van Doorslaer K, McKnight CA, Maes RK, Wise AG, Kiupel M, Van Ranst M (2006) Genetic characterization of the first chiropteran papillomavirus, isolated from a basosquamous carcinoma in an Egyptian fruit bat: the Rousettus aegyptiacus papillomavirus type 1. Vet Microbiol 117(2–4):267–275.  https://doi.org/10.1016/j.vetmic.2006.06.010 CrossRefGoogle Scholar
  53. 53.
    Canuti M, Eis-Huebinger AM, Deijs M, de Vries M, Drexler JF, Oppong SK, Müller MA, Klose SM, Wellinghausen N, Cottontail VM, Kalko EK, Drosten C, van der Hoek L (2011) Two novel parvoviruses in frugivorous New and Old World bats. PLoS One 6(12):e29140.  https://doi.org/10.1371/journal.pone.0029140 CrossRefGoogle Scholar
  54. 54.
    Ge X, Li Y, Yang X, Zhang H, Zhou P, Zhang Y, Shia Z (2012) Metagenomic analysis of viruses from bat fecal samples reveals many novel viruses in insectivorous bats in china. J Virol.  https://doi.org/10.1128/jvi.06671-11 Google Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  • Fernando Finoketti
    • 1
    Email author
  • Raíssa Nunes dos Santos
    • 1
  • Aline Alves Scarpellini Campos
    • 1
    • 2
  • André Luís da Silva Zani
    • 1
  • Camila Mosca Barboza
    • 3
  • Marcélia Emanuele Sad Fernandes
    • 3
  • Tatiane de Cassia Pardo de Souza
    • 3
  • Driele Delanira dos Santos
    • 4
  • Giovana Werneck Bortolanza
    • 4
  • Henrique Ortêncio Filho
    • 4
  • Paulo Michel Roehe
    • 1
  • Ana Cláudia Franco
    • 1
  • Helena Beatriz de Carvalho Ruthner Batista
    • 3
  1. 1.Laboratório de Virologia, Departamento de Microbiologia, Imunologia e ParasitologiaUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  2. 2.Centro Estadual de Vigilância em Saúde, Secretaria Estadual da Saúde do Rio Grande do SulPorto AlegreBrazil
  3. 3.Instituto Pasteur, Secretaria da Saúde do Governo do estado de São PauloSão PauloBrazil
  4. 4.Grupo de Estudos em Ecologia de Mamíferos e Educação AmbientalUniversidade Estadual de MaringáGoioerêBrazil

Personalised recommendations