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  • 1 Hungarian Academy of Sciences, Hungária krt. 21, H-1143 Budapest, Hungary
  • 2 Centre for Biological Threats and Special Pathogens, Berlin, Germany
  • 3 Aggtelek National Park Directorate, Jósvafő, Hungary
  • 4 Hungarian Natural History Museum, Budapest, Hungary
  • 5 Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany
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From over 1250 extant species of the order Chiroptera, 25 and 28 are known to occur in Germany and Hungary, respectively. Close to 350 samples originating from 28 bat species (17 from Germany, 27 from Hungary) were screened for the presence of adenoviruses (AdVs) using a nested PCR that targets the DNA polymerase gene of AdVs. An additional PCR was designed and applied to amplify a fragment from the gene encoding the IVa2 protein of mastadenoviruses. All German samples originated from organs of bats found moribund or dead. The Hungarian samples were excrements collected from colonies of known bat species, throat or rectal swab samples, taken from live individuals that had been captured for faunistic surveys and migration studies, as well as internal organs of dead specimens. Overall, 51 samples (14.73%) were found positive. We detected 28 seemingly novel and six previously described bat AdVs by sequencing the PCR products. The positivity rate was the highest among the guano samples of bat colonies. In phylogeny reconstructions, the AdVs detected in bats clustered roughly, but not perfectly, according to the hosts’ families (Vespertilionidae, Rhinolophidae, Hipposideridae, Phyllostomidae and Pteropodidae). In a few cases, identical sequences were derived from animals of closely related species. On the other hand, some bat species proved to harbour more than one type of AdV. The high prevalence of infection and the large number of chiropteran species worldwide make us hypothesise that hundreds of different yet unknown AdV types might circulate in bats.

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  • Anthony, S. J., Epstein, J. H., Murray, K. A., Navarrete-Macias, I., Zambrana-Torrelio, C. M., Solovyov, A., Ojeda-Flores, R., Arrigo, N. C., Islam, A., Ali Khan, S., Hosseini, P., Bogich, T. L., Olival, K. J., Sanchez-Leon, M. D., Karesh, W. B., Goldstein, T., Luby, S. P., Morse, S. S., Mazet, J. A., Daszak, P. and Lipkin, W. I. (2013): A strategy to estimate unknown viral diversity in mammals. mBio. 4, e00598-13.

    • Search Google Scholar
    • Export Citation
  • Baker, K. S. and Murcia, P. R. (2014): Poxviruses in bats… so what? Viruses 6, 15643.

  • Barr, J., Smith, C., Smith, I., de Jong, C., Todd, S., Melville, D., Broos, A., Crameri, S., Haining, J., Marsh, G., Crameri, G., Field, H. and Wang, L. F. (2015): Isolation of multiple novel paramyxoviruses from pteropid bat urine. J. Gen. Virol. 96, 243.

    • Search Google Scholar
    • Export Citation
  • Benko, M. and Harrach, B. (2003): Molecular evolution of adenoviruses. In: Doerfler, W. and Böhm P. (eds) Adenoviruses: Model and Vectors in Virus–Host Interactions, Current Topics in Microbiology and Immunology. Vol. 272. Springer, Berlin, Germany. pp. 335.

    • Search Google Scholar
    • Export Citation
  • Benko, M., Harrach, B. and Kremer, E. J. (2014): Do nonhuman primate or bat adenoviruses pose a risk for human health? Future Microbiol. 9, 2693.

    • Search Google Scholar
    • Export Citation
  • Boldogh, S. (2006): The bat fauna of the Aggtelek National Park and its surroundings (Hungary). Vespertilio 9–10, 3356.

  • Casas, I., Vazquez-Moron, S., Juste, J., Falcon, A., Aznar, C., Ibanez, C., Pozo, F., Ruiz, G., Berciano, J. M., Garin, I., Aihartza, J. M. and Echevarria, J. E. (2010): Adenovirus groups in western Palaearctic bats in Spain. GenBank Accession No. JX065117 to JX065129.

    • Search Google Scholar
    • Export Citation
  • Cavanagh, H. M., Mahony, T. J. and Vanniasinkam, T. (2012): Genetic characterization of equine adenovirus type 1. Vet. Microbiol. 155, 333.

    • Search Google Scholar
    • Export Citation
  • Chen, L. H., Wu, Z. Q., Hu, Y. F., Yang, F., Yang, J. and Jin, Q. (2012): Genetic diversity of adenoviruses in bats of China [in Chinese]. Bing Du Xue Bao 28, 4033.

    • Search Google Scholar
    • Export Citation
  • Dandár, E., Szabó, L., Heltai, M. and Doszpoly, A. (2010): PCR screening of mammalian predators (Carnivora) for adenoviruses and herpesviruses: the first detection of a mustelid herpesvirus in Hungary [in Hungarian, with English abstract]. Magyar Állatorvosok Lapja 132, 3023.

    • Search Google Scholar
    • Export Citation
  • Davison, A. J., Benko, M. and Harrach, B. (2003): Genetic content and evolution of adenoviruses. J. Gen. Virol. 84, 28953.

  • Davison, A. J., Wright, K. M. and Harrach, B. (2000): DNA sequence of frog adenovirus. J. Gen. Virol. 81, 24313.

  • Doszpoly, A., Tarján, Z. L., Glávits, R., Müller, T. and Benko, M. (2014): Full genome sequence of a novel circo-like virus detected in an adult European eel Anguilla anguilla showing signs of cauliflower disease. Dis. Aquat. Organ. 109, 1073.

    • Search Google Scholar
    • Export Citation
  • Doszpoly, A., Wellehan, J. F. X., Childress, A. L., Tarján, Z. L., Kovács, E. R., Harrach, B. and Benko, M. (2013): Partial characterization of a new adenovirus lineage discovered in testudinoid turtles. Infect. Genet. Evol. 17, 1063.

    • Search Google Scholar
    • Export Citation
  • Drexler, J. F., Corman, V. M., Wegner, T., Tateno, A. F., Zerbinati, R. M., Gloza-Rausch, F., Seebens, A., Müller, M. A. and Drosten, C. (2011): Amplification of emerging viruses in a bat colony. Emerg. Infect. Dis. 17, 4493.

    • Search Google Scholar
    • Export Citation
  • Evans, P. S., Benko, M., Harrach, B. and Letchworth, G. J. (1998): Sequence, transcriptional analysis, and deletion of the bovine adenovirus type 1 E3 region. Virology 244, 1733.

    • Search Google Scholar
    • Export Citation
  • Farkas, S. L. and Gál, J. (2009): Adenovirus and mycoplasma infection in an ornate box turtle (Terrapene ornata ornata) in Hungary. Vet. Microbiol. 138, 1693.

    • Search Google Scholar
    • Export Citation
  • Farkas, S. L., Harrach, B. and Benko, M. (2008): Completion of the genome analysis of snake adenovirus type 1, a representative of the reptilian lineage within the novel genus Atadenovirus. Virus Res. 132, 1323.

    • Search Google Scholar
    • Export Citation
  • Gál, J., Hornyák, Á., Mándoki, M., Bakonyi, T., Balka, G., Szeredi, L., Marosán, M., Ludányi, T., Forgách, P., Sós, E., Demeter, Z. and Farkas, S. L. (2013): Novel mastadenovirus infection and clinical disease in a pygmy marmoset (Callithrix [Cebuella] pygmaea). Vet. Microbiol. 167, 6953.

    • Search Google Scholar
    • Export Citation
  • Harrach, B. and Benko, M. (2007): Phylogenetic analysis of adenovirus sequences. In: Wold, W. S. M. and Tollefson, A. E. (eds) Adenovirus Methods and Protocols. Second Edition. Humana Press, Totowa, NJ, USA. pp. 299334.

    • Search Google Scholar
    • Export Citation
  • Harrach, B., Benko, M., Both, G. W., Brown, M., Davison, A. J., Echavarría, M., Hess, M., Jones, M. S., Kajon, A., Lehmkuhl, A. D., Mautner, V., Mittal, S. K. and Wadell, G. (2011): Family Adenoviridae. In: King, A. M. Q., Adams, M. J., Carstens, E. B. and Lefkowitz, E. J. (eds) Virus Taxonomy: Classification and Nomenclature of Viruses. Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier, San Diego, USA. pp. 125141.

    • Search Google Scholar
    • Export Citation
  • Hutterer, R., Ivanova, T., Meyer-Cords, C. and Rodrigues, L. (2005): Bat Migrations in Europe –A Review of Banding Data and Literature. Bonn: Budesamt für Naturschutz. 180 pp.

  • Jánoska, M., Vidovszky, M., Molnár, V., Liptovszky, M., Harrach, B. and Benko, M. (2011): Novel adenoviruses and herpesviruses detected in bats. Vet. J. 189, 1183.

    • Search Google Scholar
    • Export Citation
  • Juste, J., Benda, P., Garcia-Mudarra, J. J. and Ibánez, C. (2013): Phylogeny and systematics of Old World serotine bats (genus Eptesicus, Vespertilionidae, Chiroptera): an integrative approach. Zool. Scr. 42, 4413.

    • Search Google Scholar
    • Export Citation
  • Kaján, G. L., Sameti, S. and Benko, M. (2011): Partial sequence of the DNA-dependent DNA polymerase gene of fowl adenoviruses: a reference panel for a general diagnostic PCR in poultry. Acta Vet. Hung. 59, 2793.

    • Search Google Scholar
    • Export Citation
  • Kajon, A. E., Dickson, L. M., Murtagh, P., Viale, D., Carballal, G. and Echavaria, M. (2010): Molecular characterization of an adenovirus 3–16 intertypic recombinant isolated in Argentina from an infant hospitalized with acute respiratory infection. J. Clin. Microbiol. 4, 14943.

    • Search Google Scholar
    • Export Citation
  • Kohl, C. and Kurth, A. (2014): European bats as carriers of viruses with zoonotic potential. Viruses 6, 31103.

  • Kohl, C., Vidovszky, M. Z., Mühldorfer, K., Dabrowski, P. W., Radonic, A., Nitsche, A., Wibbelt, G., Kurth, A. and Harrach, B. (2012): Genome analysis of bat adenovirus 2: indications of interspecies transmission. J. Virol. 86, 18883.

    • Search Google Scholar
    • Export Citation
  • Kovács, E. R. and Benko, M. (2011): Complete sequence of raptor adenovirus 1 confirms the characteristic genome organization of siadenoviruses. Infect. Genet. Evol. 11, 10583.

    • Search Google Scholar
    • Export Citation
  • Kovács, E. R., Jánoska, M., Dán, A., Harrach, B. and Benko, M. (2009): Recognition and partial genome characterization by non-specific DNA amplification and PCR of a new siadenovirus species in a sample originating from Parus major, a great tit. J. Virol. Methods 163, 2623.

    • Search Google Scholar
    • Export Citation
  • Li, L., Victoria, J. G., Wang, C., Jones, M., Fellers, G. M., Kunz, T. H. and Delwart, E. (2010a): Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. J. Virol. 84, 69553.

    • Search Google Scholar
    • Export Citation
  • Li, Y., Ge, X., Zhang, H., Zhou, P., Zhu, Y., Zhang, Y., Yuan, J., Wang, L. F. and Shi, Z. (2010b): Host range, prevalence, and genetic diversity of adenoviruses in bats. J. Virol. 84, 38893.

    • Search Google Scholar
    • Export Citation
  • Lima, F. E., Cibulski, S. P., Elesbao, F., Carnieli Junior, P., Batista, H. B., Roehe, P. M. and Franco, A. C. (2013): First detection of adenovirus in the vampire bat (Desmodus rotundus) in Brazil. Virus Genes 47, 3783.

    • Search Google Scholar
    • Export Citation
  • Maeda, K., Hondo, E., Terakawa, J., Kiso, Y., Nakaichi, N., Endoh, D., Sakai, K., Morikawa, S. and Mizutani, T. (2008): Isolation of novel adenovirus from fruit bat (Pteropus dasymallus yayeyamae). Emerg. Infect. Dis. 14, 3473.

    • Search Google Scholar
    • Export Citation
  • Papp, T., Fledelius, B., Schmidt, V., Kaján, G. L. and Marschang, R. E. (2009): PCR-sequence characterization of new adenoviruses found in reptiles and the first successful isolation of a lizard adenovirus. Vet. Microbiol. 134, 2333.

    • Search Google Scholar
    • Export Citation
  • Pardo-Mateos, A. and Young, C. S. H. (2004): Adenovirus IVa2 protein plays an important role in transcription from the major late promoter in vivo. Virology 327, 503.

    • Search Google Scholar
    • Export Citation
  • Park, Y. M., Kim, J. H., Gu, S. H., Lee, S. Y., Lee, M. G., Kang, Y. K., Kang, S. H., Kim, H. J. and Song, J. W. (2012): Full genome analysis of a novel adenovirus from the South Polar skua (Catharacta maccormicki) in Antarctica. Virology 422, 1443.

    • Search Google Scholar
    • Export Citation
  • Raut, C. G., Yadav, P. D., Towner, J., Amman, B. R., Erickson, B. R., Cannon, D. L., Sivaram, A., Basu, A., Nichol, S. T., Mishra, A. C. and Mourya, D. T. (2012): Isolation of a novel adenovirus from Rousettus leschenaultii bats from India. Intervirology 55, 4883.

    • Search Google Scholar
    • Export Citation
  • Reagan, R. L., Smith, E. J. and Brueckner, A. L. (1950): Studies of Newcastle disease virus (NDV) propagated in the cave bat (Myotus lucifugus). Proc. Soc. Exp. Biol. Med. 75, 6913.

    • Search Google Scholar
    • Export Citation
  • Reuter, G., Pankovics, P., Gyöngyi, Z., Delwart, E. and Boros, A. (2014): Novel dicistrovirus from bat guano. Arch. Virol. 159, 34533.

    • Search Google Scholar
    • Export Citation
  • Rivera, S., Wellehan, J. F., McManamon, R., Innis, C. J., Garner, M. M., Raphael, B. L., Gregory, C. R., Latimer, K. S., Rodriguez, C. E., Diaz-Figueroa, O., Marlar, A. B., Nyaoke, A., Gates, A. E., Gilbert, K., Childress, A. L., Risatti, G. R. and Frasca, S. (2009): Systemic adenovirus infection in Sulawesi tortoises (Indotestudo forsteni) caused by a novel siadenovirus. J. Vet. Diagn. Invest. 21, 4153.

    • Search Google Scholar
    • Export Citation
  • Schumacher, V. L., Innis, C. J., Garner, M. M., Risatti, G. R., Nordhausen, R. W., Gilbert- Marcheterre, K., Wellehan, J. F. Jr., Childress, A. L. and Frasca, S. (2012): Sulawesi tortoise adenovirus-1 in two impressed tortoises (Manouria impressa) and a Burmese star tortoise (Geochelone platynota). J. Zoo Wildl. Med. 43, 5013.

    • Search Google Scholar
    • Export Citation
  • Sonntag, M., Mühldorfer, K., Speck, S., Wibbelt, G. and Kurth, A. (2009): New adenovirus in bats, Germany. Emerg. Infect. Dis. 15, 20523.

    • Search Google Scholar
    • Export Citation
  • Ursu, K., Harrach, B., Matiz, K. and Benko, M. (2004): DNA sequencing and analysis of the righthand part of the genome of the unique bovine adenovirus type 10. J. Gen. Virol. 85, 5933.

    • Search Google Scholar
    • Export Citation
  • van der Poel, W. H., Lina, P. H. and Kramps, J. A. (2006): Public health awareness of emerging zoonotic viruses of bats: a European perspective. Vector Borne Zoonotic Dis. 6, 3153.

    • Search Google Scholar
    • Export Citation
  • Vidovszky, M. Z. and Boldogh, S. (2011): Detection of adenoviruses in the Northern Hungarian bat fauna [in Hungarian, with English abstract]. Magyar Állatorvosok Lapja 133, 7473.

    • Search Google Scholar
    • Export Citation
  • Wellehan, J. F. X., Johnson, A. J., Harrach, B., Benko, M., Pessier, A. P., Johnson, C. M., Garner, M. M., Childress, A. and Jacobson, E. R. (2004): Detection and analysis of six lizard adenoviruses by consensus primer PCR provides further evidence of a reptilian origin for the atadenoviruses. J. Virol. 78, 133663.

    • Search Google Scholar
    • Export Citation
  • Yang, F., Wang, Y., Zheng, W., He, B., Jiang, T., Li, Y., Xia, L., Feng, Y., Fan, Q. and Tu, C. (2013): Metagenomic analysis of bat virome in several Chinese regions [in Chinese]. Sheng Wu Gong Cheng Xue Bao 29, 5863.

    • Search Google Scholar
    • Export Citation

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