View More View Less
  • 1 Hungarian Academy of Sciences, Budapest, Hungary
  • 2 Wageningen University, the Netherlands
  • 3 Budapest Zoo and Botanical Garden, Budapest, Hungary
  • 4 Zoo de Montpellier, Montpellier, France
  • a Ruđer Bošković Institute, Zagreb, Croatia
  • b Hokkaido University, Sapporo, Japan
  • c Ankara University Veterinary Faculty, Ankara, Turkey
Open access

The scarcity or complete lack of information on the adenoviruses (AdVs) occurring in the most ancient non-human primates resulted in the initiation of a study for exploring their abundance and diversity in prosimians and New World monkeys (NWMs). In order to assess the variability of these AdVs and the possible signs of the hypothesised virus−host co-evolution, samples from almost every family of NWMs and prosimians were screened for the presence of AdVs. A PCRscreening of 171 faecal or organ samples from live or dead, captive or wild-living prosimians and NWMs was performed. The PCR products from the gene of the IVa2 protein were sequenced and used in phylogeny calculations. The presence of 10 and 15 new AdVs in seven and ten different species of prosimians and NWMs was revealed, respectively. Phylogenetic analysis indicated that the tentative novel AdVs cluster into two separate groups, which form the most basal branches among the primate AdVs, and therefore support the theory on the co-evolution of primate AdVs with their hosts. This is the first report that provides a comprehensive overview of the AdVs occurring in prosimians and NWMs, and the first insight into the evolutionary relationships among AdVs from all major primate groups.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Adams, M. J., Lefkowitz, E. J., King, A. M. Q., Harrach, B., Harrison, R. L., Knowles, N. J., Kropinski, A. M., Krupovic, M., Kuhn, J. H., Mushegian, A. R., Nibert, M., Sabanadzovic, S., Sanfaçon, H., Siddell, S. G., Simmonds, P., Varsani, A., Zerbini, F. M., Gorbalenya, A. E. and Davison, A. J. (2017): Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2017). Arch. Virol. 162, 25052538.

    • Search Google Scholar
    • Export Citation
  • Ballmann, M. Z. and Harrach, B. (2016): Detection and partial genetic characterisation of novel avi- and siadenoviruses in racing and fancy pigeons (Columba livia domestica). Acta Vet. Hung. 64, 514528.

    • Search Google Scholar
    • Export Citation
  • Chen, E. C., Yagi, S., Kelly, K. R., Mendoza, S. P., Tarara, R. P., Canfield, D. R., Maninger, N., Rosenthal, A., Spinner, A., Bales, K. L., Schnurr, D. P., Lerche, N. W. and Chiu, C. Y. (2011): Cross-species transmission of a novel adenovirus associated with a fulminant pneumonia outbreak in a new world monkey colony. PLoS Pathog. 7, e1002155.

    • Search Google Scholar
    • Export Citation
  • Chiu, C. Y., Yagi, S., Lu, X., Yu, G., Chen, E. C., Liu, M., Dick, E. J., Carey, K. D., Erdman, D. D., Leland, M. M. and Patterson, J. L. (2013): A novel adenovirus species associated with an acute respiratory outbreak in a baboon colony and evidence of coincident human infection. MBio. 4, e00084.

    • Search Google Scholar
    • Export Citation
  • Crawford-Miksza, L. K. and Schnurr, D. P. (1996): Adenovirus serotype evolution is driven by illegitimate recombination in the hypervariable regions of the hexon protein. Virology 224, 357367.

    • Search Google Scholar
    • Export Citation
  • Dehghan, S., Seto, J., Jones, M. S., Dyer, D. W., Chodosh, J. and Seto, D. (2013): Simian adenovirus type 35 has a recombinant genome comprising human and simian adenovirus sequences, which predicts its potential emergence as a human respiratory pathogen. Virology 447, 265273.

    • Search Google Scholar
    • Export Citation
  • Doszpoly, A., Tarján, Z. L., Glávits, R., Müller, T. and Benkő, 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, 107115.

    • Search Google Scholar
    • Export Citation
  • Doszpoly, A., Wellehan, J. F., Childress, A. L., Tarján, Z. L., Kovács, E. R., Harrach, B. and Benkő, M. (2013): Partial characterization of a new adenovirus lineage discovered in testudinoid turtles. Infect Genet. Evol. 17, 106112.

    • 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, 695699.

    • Search Google Scholar
    • Export Citation
  • Hall, N. H., Archer, L. L., Childress, A. L. and Wellehan, J. F. (2012): Identification of a novel adenovirus in a cotton-top tamarin (Saguinus oedipus). J. Vet. Diagn. Invest. 24, 359363.

    • Search Google Scholar
    • Export Citation
  • Harrach, B. (2014) Adenoviruses: General features. In: Caplan, M., Mitchell, R., Bradshaw, R. and McManus, L. (eds) Reference Module in Biomedical Sciences. Elsevier, Amsterdam. pp. 19.

    • Search Google Scholar
    • Export Citation
  • Harrach, B. and Benkő, M. (2007): Phylogenetic analysis of adenovirus sequences. Methods Mol. Med. 131, 299334.

  • Harrach, B., Benkő, M., Both, G. W., Brown, M., Davison, A. J., Echavarria, M., Hess, M., Jones, M. S., Kajon, A., Lehmkuhl, H. D., Mautner, V., Mittal, S. K. and Wadell, G. (2011): Family Adenoviridae. In: King, A. M. Q., Adams, M. J., Lefkowitz, E. and Carstens, E. B. (eds) Virus Taxonomy. Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier, Oxford. pp. 125141.

    • Search Google Scholar
    • Export Citation
  • Jones, M. S., Harrach, B., Ganac, R. D., Gozum, M. M., Dela Cruz, W. P., Riedel, B., Pan, C., Delwart, E. L. and Schnurr, D. P. (2007): New adenovirus species found in a patient presenting with gastroenteritis. J. Virol. 81, 59785984.

    • Search Google Scholar
    • Export Citation
  • Jánoska, M., Vidovszky, M., Molnár, V., Liptovszky, M., Harrach, B. and Benkő, M. (2011): Novel adenoviruses and herpesviruses detected in bats. Vet. J. 189, 118121.

    • Search Google Scholar
    • Export Citation
  • Kohl, C., Vidovszky, M. Z., Mühldorfer, K., Dabrowski, P. W., Radonić, A., Nitsche, A., Wibbelt, G., Kurth, A. and Harrach, B. (2012): Genome analysis of bat adenovirus 2: indications of interspecies transmission. J. Virol. 86, 18881892.

    • Search Google Scholar
    • Export Citation
  • Kovács, G. M., Davison, A. J., Zakhartchouk, A. N. and Harrach, B. (2004): Analysis of the first complete genome sequence of an Old World monkey adenovirus reveals a lineage distinct from the six human adenovirus species. J. Gen. Virol. 85, 27992807.

    • Search Google Scholar
    • Export Citation
  • Kozak, R. A., Ackford, J. G., Slaine, P., Li, A., Carman, S., Campbell, D., Welch, M. K., Kropinski, A. M. and Nagy, É. (2015): Characterization of a novel adenovirus isolated from a skunk. Virology 485, 1624.

    • Search Google Scholar
    • Export Citation
  • Lakatos, B., Hornyák, Á., Demeter, Z., Forgách, P., Kennedy, F. and Rusvai, M. (2017): Detection of a putative novel adenovirus by PCR amplification, sequencing and phylogenetic characterisation of two gene fragments from formalin-fixed paraffin-embedded tissues of a cat diagnosed with disseminated adenovirus disease. Acta Vet. Hung. 65, 574584.

    • Search Google Scholar
    • Export Citation
  • Madarame, H., Ogihara, K., Ochia, H., Omatsu, T. and Mizutani, T. (2016): Detection of skunk adenovirus 1 (SkAdV-1) in an African pigmy hedgehog (Atelerix albiventris). Vet. Rec. Case Reports 4, e000321.

    • Search Google Scholar
    • Export Citation
  • Malouli, D., Howell, G. L., Legasse, A. W., Kahl, C., Axthelm, M. K., Hansen, S. G. and Früh, K. (2014): Full genome sequence analysis of a novel adenovirus of rhesus macaque origin indicates a new simian adenovirus type and species. Virol. Rep. 3−4, 1829.

    • Search Google Scholar
    • Export Citation
  • Pantó, L., Podgorski, I. I., Jánoska, M., Márkó, O. and Harrach, B. (2015): Taxonomy proposal for Old World monkey adenoviruses: characterisation of several non-human, non-ape primate adenovirus lineages. Arch. Virol. 160, 31653177.

    • Search Google Scholar
    • Export Citation
  • Perelman, P., Johnson, W. E., Roos, C., Seuánez, H. N., Horvath, J. E., Moreira, M. A., Kessing, B., Pontius, J., Roelke, M., Rumpler, Y., Schneider, M. P., Silva, A., O’Brien, S. J. and Pecon-Slattery, J. (2011): A molecular phylogeny of living primates. PLoS Genet. 7, e1001342.

    • Search Google Scholar
    • Export Citation
  • Podgorski, I. I., Pantó, L., Papp, T., Harrach, B. and Benkő, M. (2016): Genome analysis of four Old World monkey adenoviruses supports the proposed species classification of primate adenoviruses and reveals signs of possible homologous recombination. J. Gen. Virol. 97, 16041614.

    • Search Google Scholar
    • Export Citation
  • Roos, C. and Zinner, D. (2017): Primate phylogeny. In: Bezanson, M., MacKinnon, K. C., Riley, E., Campbell, C. J., Nekaris, K. A. I., Estrada, A., Di Fiore, A. F., Ross, S., Jones-Engel, L. E., Thierry, B., Sussman, R. W., Sanz, C., Loudon, J., Elton, S. and Fuentes, A. (eds) The International Encyclopedia of Primatology. John Wiley & Sons, Inc., USA, pp. 10631068.

    • Search Google Scholar
    • Export Citation
  • Roy, S., Sandhu, A., Medina, A., Clawson, D. S. and Wilson, J. M. (2012): Adenoviruses in fecal samples from asymptomatic rhesus macaques, United States, Emerg. Infect. Dis. 18, 10811088.

    • Search Google Scholar
    • Export Citation
  • Shroyer, E. L., Kelley, S. T., Taylor, P. C., Vanderloo, P. and Lester, T. L. (1979): Three serologic types of adenovirus infections of owl monkeys. Am. J. Vet. Res. 40, 532536.

    • Search Google Scholar
    • Export Citation
  • Tan, B., Wu, L. J., Yang, X. L., Li, B., Zhang, W., Lei, Y. S., Li, Y., Yang, G. X., Chen, J., Chen, G., Wang, H. Z. and Shi, Z. L. (2016): Isolation and characterization of adenoviruses infecting endangered golden snub-nosed monkeys (Rhinopithecus roxellana). Virol. J. 13, 190.

    • Search Google Scholar
    • Export Citation
  • Vidovszky, M., Kohl, C., Boldogh, S., Görföl, T., Wibbelt, G., Kurth, A. and Harrach, B. (2015): Random sampling of the Central European bat fauna reveals the existence of numerous hitherto unknown adenoviruses. Acta Vet. Hung. 63, 508525.

    • Search Google Scholar
    • Export Citation
  • Walsh, M. P., Seto, J., Liu, E. B., Dehghan, S., Hudson, N. R., Lukashev, A. N., Ivanova, O., Chodosh, J., Dyer, D. W., Jones, M. S. and Seto, D. (2011): Computational analysis of two species C human adenoviruses provides evidence of a novel virus. J. Clin. Microbiol. 49, 34823490.

    • Search Google Scholar
    • Export Citation
  • Wevers, D., Metzger, S., Babweteera, F., Bieberbach, M., Boesch, C., Cameron, K., Couacy-Hymann, E., Cranfield, M., Gray, M., Harris, L. A., Head, J., Jeffery, K., Knauf, S., Lankester, F., Leendertz, S. A., Lonsdorf, E., Mugisha, L., Nitsche, A., Reed, P., Robbins, M., Travis, D. A., Zommers, Z., Leendertz, F. H. and Ehlers, B. (2011): Novel adenoviruses in wild primates: a high level of genetic diversity and evidence of zoonotic transmissions. J. Virol. 85, 1077410784.

    • Search Google Scholar
    • Export Citation
  • Yu, G., Yagi, S., Carrion, R., Chen, E. C., Liu, M., Brasky, K. M., Lanford, R. E., Kelly, K. R., Bales, K. L., Schnurr, D. P., Canfield, D. R., Patterson, J. L. and Chiu, C. Y. (2013): Experimental cross-species infection of common marmosets by titi monkey adenovirus. PLoS One 8, e68558.

    • Search Google Scholar
    • Export Citation

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Jun 2020 0 11 6
Jul 2020 0 16 7
Aug 2020 0 13 6
Sep 2020 0 8 4
Oct 2020 0 17 17
Nov 2020 0 12 8
Dec 2020 0 0 0