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Abstract

Adenoviruses (AdVs) are diverse pathogens of humans and animals, with several dozen bat AdVs already identified. Considering that over 100 human AdVs are known, and the huge diversity of bat species, many bat AdVs likely remain undiscovered. To learn more about AdV prevalence, diversity and evolution, we sampled and tested bats in Cameroon using several PCR assays for viral and host DNA. AdV DNA was detected in 14 % of the 671 sampled animals belonging to 37 different bat species. There was a correlation between species roosting in larger groups and AdV DNA detection. The detected AdV DNA belonged to between 28 and 44 different, mostly previously unknown, mastadenovirus species. The novel isolates are phylogenetically diverse and while some cluster with known viruses, others appear to form divergent new clusters. The phylogenetic tree of novel and previously known bat AdVs does not mirror that of the various host species, but does contain structures consistent with a degree of virus–host co-evolution. Given that closely related isolates were found in different host species, it seems likely that at least some bat AdVs have jumped species barriers, probably in the more recent past; however, the tree is also consistent with such events having taken place throughout bat AdV evolution. AdV diversity was highest in bat species roosting in large groups. The study significantly increased the diversity of AdVs known to be harboured by bats, and suggests that host behaviours, such as roosting size, may be what limits some AdVs to one species rather than an inability of AdVs to infect other related hosts.

Funding
This study was supported by the:
  • Fogarty International Center (Award K01 TW00003-1)
    • Principle Award Recipient: NathanD. Wolfe
  • Foundation for the National Institutes of Health (Award DP1-OD000370)
    • Principle Award Recipient: NathanD. Wolfe
  • United States Agency for International Development (Award GHN-A-OO-09-00010-00)
    • Principle Award Recipient: NathanD. Wolfe
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2021-04-19
2024-04-19
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References

  1. Purkayastha A, Ditty SE, Su J, McGraw J, Hadfield TL et al. Genomic and bioinformatics analysis of HAdV-4, a human adenovirus causing acute respiratory disease: implications for gene therapy and vaccine vector development. J Virol 2005; 79:2559–2572 [View Article][PubMed]
    [Google Scholar]
  2. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. Virus Taxonomy: Classification and Nomenclature of Viruses. Ninth Report of the International Committee on Taxonomy of Viruses Amsterdam: Elsevier Academic Press; 2012
    [Google Scholar]
  3. Berk AJ. Adenoviridae. In Knipe DM, Howley PM. eds Fields Virology, 6th edn. Philadelphia: Lippincott Williams and Wilkins; 2013 pp 1704–1731
    [Google Scholar]
  4. Wold WSM, Ison MG. Adenoviruses. In Knipe DM, Howley PM. eds Fields Virology, 6th edn. Philadelphia: Lippincott Williams and Wilkins; 2013 pp 1732–1767
    [Google Scholar]
  5. Benkö M, Harrach B. Molecular evolution of adenoviruses. Curr Top Microbiol Immunol 2003; 272:3–35 [View Article][PubMed]
    [Google Scholar]
  6. Chen EC, Yagi S, Kelly KR, Mendoza SP, Tarara RP et al. Cross-species transmission of a novel adenovirus associated with a fulminant pneumonia outbreak in a new world monkey colony. PLoS Pathog 2011; 7:e1002155 [View Article][PubMed]
    [Google Scholar]
  7. Balboni A, Verin R, Morandi F, Poli A, Prosperi S et al. Molecular epidemiology of canine adenovirus type 1 and type 2 in free-ranging red foxes (Vulpes vulpes) in Italy. Vet Microbiol 2013; 162:551–557 [View Article][PubMed]
    [Google Scholar]
  8. Dehghan S, Seto J, Liu EB, Walsh MP, Dyer DW et al. Computational analysis of four human adenovirus type 4 genomes reveals molecular evolution through two interspecies recombination events. Virology 2013; 443:197–207 [View Article][PubMed]
    [Google Scholar]
  9. Dehghan S, Seto J, Liu EB, Ismail AM, Madupu R et al. A zoonotic adenoviral human pathogen emerged through genomic recombination among human and nonhuman simian hosts. J Virol 2019; 93:e00564-19 [View Article][PubMed]
    [Google Scholar]
  10. Lange CE, Niama FR, Cameron K, Olsen SH, Aime Nina R et al. First evidence of a new simian adenovirus clustering with human mastadenovirus F viruses. Virol J 2019; 16:147 [View Article][PubMed]
    [Google Scholar]
  11. Zheng X-Y, Qiu M, Ke X-M, Guan W-J, Li J-M et al. Detection of novel adenoviruses in fecal specimens from rodents and shrews in southern China. Virus Genes 2016; 52:417–421 [View Article][PubMed]
    [Google Scholar]
  12. Diffo J, Ndze VN, Ntumvi NF, Takuo J-M, Mouiche MMM et al. DNA of diverse adenoviruses detected in Cameroonian rodent and shrew species. Arch Virol 2019; 164:2359–2366 [View Article][PubMed]
    [Google Scholar]
  13. Kumakamba C, N'Kawa F, Kingebeni PM, Losoma JA, Lukusa IN et al. Analysis of adenovirus DNA detected in rodent species from the Democratic Republic of the Congo indicates potentially novel adenovirus types. New Microbes New Infect 2020; 34:100640 [View Article][PubMed]
    [Google Scholar]
  14. Vidovszky M, Kohl C, Boldogh S, Görföl T, Wibbelt G et al. Random sampling of the central European bat fauna reveals the existence of numerous hitherto unknown adenoviruses. Acta Vet Hung 2015; 63:508–525 [View Article][PubMed]
    [Google Scholar]
  15. Tan B, Yang XL, Ge X-Y, Peng C, Liu H-Z et al. Novel bat adenoviruses with low G+C content shed new light on the evolution of adenoviruses. J Gen Virol 2017; 98:739–748 [View Article][PubMed]
    [Google Scholar]
  16. Sonntag M, Mühldorfer K, Speck S, Wibbelt G, Kurth A. New adenovirus in bats, Germany. Emerg Infect Dis 2009; 15:2052–2055 [View Article][PubMed]
    [Google Scholar]
  17. Li Y, Ge X, Zhang H, Zhou P, Zhu Y et al. Host range, prevalence, and genetic diversity of adenoviruses in bats. J Virol 2010; 84:3889–3897 [View Article][PubMed]
    [Google Scholar]
  18. Jánoska M, Vidovszky M, Molnár V, Liptovszky M, Harrach B et al. Novel adenoviruses and herpesviruses detected in bats. Vet J 2011; 189:118–121 [View Article][PubMed]
    [Google Scholar]
  19. Raut CG, Yadav PD, Towner JS, Amman BR, Erickson BR et al. Isolation of a novel adenovirus from Rousettus leschenaultii bats from India. Intervirology 2012; 55:488–490 [View Article][PubMed]
    [Google Scholar]
  20. Hu D, Zhu C, Wang Y, Ai L, Yang L et al. Virome analysis for identification of novel mammalian viruses in bats from Southeast China. Sci Rep 2017; 7:10917 [View Article][PubMed]
    [Google Scholar]
  21. Ogawa H, Kajihara M, Nao N, Shigeno A, Fujikura D et al. Characterization of a novel bat adenovirus isolated from straw-colored fruit bat (Eidolon helvum). Viruses 2017; 9:371 [View Article]
    [Google Scholar]
  22. Iglesias-Caballero M, Juste J, Vázquez-Morón S, Falcon A, Aznar-Lopez C et al. New adenovirus groups in Western Palaearctic bats. Viruses 2018; 10:443 [View Article][PubMed]
    [Google Scholar]
  23. Kohl C, Vidovszky MZ, Mühldorfer K, Dabrowski PW, Radonić A et al. Genome analysis of bat adenovirus 2: indications of interspecies transmission. J Virol 2012; 86:1888–1892 [View Article][PubMed]
    [Google Scholar]
  24. Podgorski II, Pantó L, Földes K, de Winter I, Jánoska M et al. Adenoviruses of the most ancient primate lineages support the theory on virus-host co-evolution. Acta Vet Hung 2018; 66:474–487 [View Article][PubMed]
    [Google Scholar]
  25. Wellehan JF, Johnson AJ, Harrach B, Benkö M, Pessier AP et al. Detection and analysis of six lizard adenoviruses by consensus primer PCR provides further evidence of a reptilian origin for the atadenoviruses. J Virol 2004; 78:13366–13369 [View Article][PubMed]
    [Google Scholar]
  26. Townzen JS, Brower AV, Judd DD. Identification of mosquito bloodmeals using mitochondrial cytochrome oxidase subunit I and cytochrome b gene sequences. Med Vet Entomol 2008; 22:386–393 [View Article][PubMed]
    [Google Scholar]
  27. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 2012; 61:539–542 [View Article][PubMed]
    [Google Scholar]
  28. Rosevear DR. The Bats of West Africa London: British Museum (Natural History); 1965
    [Google Scholar]
  29. Monadjem A, Taylor PJ, Cotterill W, Schoeman MC. Bats of Southern and Central Africa: a Biogeographic and Taxonomic Synthesis Johannesburg: Wits University Press; 2010 p 596
    [Google Scholar]
  30. Wilson DE, Mittermeier RA. Handbook of the Mammals of the World, vol. 9, Bats Barcelona: Lynx; 2019
    [Google Scholar]
  31. Conow C, Fielder D, Ovadia Y, Libeskind-Hadas R. Jane: a new tool for the cophylogeny reconstruction problem. Algorithms Mol Biol 2010; 5:16 [View Article][PubMed]
    [Google Scholar]
  32. Parker J, Rambaut A, Pybus OG. Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. Infect Genet Evol 2008; 8:239–246 [View Article][PubMed]
    [Google Scholar]
  33. Laughlin AJ, Hall RJ, Taylor CM. Ecological determinants of pathogen transmission in communally roosting species. Theor Ecol 2019; 12:225–235 [View Article]
    [Google Scholar]
  34. Rahman SA, Hassan L, Epstein JH, Mamat ZC, Yatim AM et al. Risk factors for Nipah virus infection among pteropid bats, Peninsular Malaysia. Emerg Infect Dis 2013; 19:51–60 [View Article][PubMed]
    [Google Scholar]
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