1887

Abstract

Bats have been reported to carry diverse adenoviruses. However, most bat adenoviruses have been identified on the basis of partial genome sequences, and knowledge on the evolution of bat adenoviruses remains limited. In this study, we isolated and characterized four novel adenoviruses from two distinct bat species, and their full-length genomes were sequenced. Sequence analysis revealed that these isolates represented three distinct species of the genus Mastadenovirus. However, all isolates had an exceptionally low G+C content and relatively short genomes compared with other known mastadenoviruses. We further analysed the relationships among the G+C content, 5′-C-phosphate-G-3′ (CpG) representation and genome size in the family Adenoviridae. Our results revealed that the CpG representation in adenoviral genomes depends primarily on the level of methylation, and the genome size displayed significant positive correlations with both G+C content and CpG representation. Since ancestral adenoviruses are believed to have contained short genomes, those probably had a low G+C content, similar to the genomes of these bat strains. Our results suggest that bats are important natural reservoirs for adenoviruses and play important roles in the evolution of adenoviruses.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000739
2017-05-05
2019-10-15
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/4/739.html?itemId=/content/journal/jgv/10.1099/jgv.0.000739&mimeType=html&fmt=ahah

References

  1. Harrach B, Benkö M, Both GW, Brown M, Davison AJ et al. Family Adenoviridae. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. (editors) Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses San Diego: Elsevier; 2011; pp.125–141
    [Google Scholar]
  2. Cortés-Hinojosa G, Gulland FM, Goldstein T, Venn-Watson S, Rivera R et al. Phylogenomic characterization of California sea lion adenovirus-1. Infect Genet Evol 2015;31:270–276 [CrossRef][PubMed]
    [Google Scholar]
  3. Benkö M, Harrach B. Molecular evolution of adenoviruses. Curr Top Microbiol Immunol 2003;272:3–35[PubMed]
    [Google Scholar]
  4. Davison AJ, Akter P, Cunningham C, Dolan A, Addison C et al. Homology between the human cytomegalovirus RL11 gene family and human adenovirus E3 genes. J Gen Virol 2003;84:657–663 [CrossRef][PubMed]
    [Google Scholar]
  5. Singh G, Robinson CM, Dehghan S, Jones MS, Dyer DW et al. Homologous recombination in E3 genes of human adenovirus species D. J Virol 2013;87:12481–12488 [CrossRef][PubMed]
    [Google Scholar]
  6. Mugal CF, Arndt PF, Holm L, Ellegren H. Evolutionary consequences of DNA methylation on the GC content in vertebrate genomes. G3 (Bethesda) 2015;5:441–447 [CrossRef][PubMed]
    [Google Scholar]
  7. Galtier N, Piganeau G, Mouchiroud D, Duret L. GC-content evolution in mammalian genomes: the biased gene conversion hypothesis. Genetics 2001;159:907–911[PubMed]
    [Google Scholar]
  8. Wolfe KH, Sharp PM, Li WH. Mutation rates differ among regions of the mammalian genome. Nature 1989;337:283–285 [CrossRef][PubMed]
    [Google Scholar]
  9. Fryxell KJ, Zuckerkandl E. Cytosine deamination plays a primary role in the evolution of mammalian isochores. Mol Biol Evol 2000;17:1371–1383 [CrossRef][PubMed]
    [Google Scholar]
  10. Duret L, Galtier N. The covariation between TpA deficiency, CpG deficiency, and G+C content of human isochores is due to a mathematical artifact. Mol Biol Evol 2000;17:1620–1625 [CrossRef][PubMed]
    [Google Scholar]
  11. Karlin S, Doerfler W, Cardon LR. Why is CpG suppressed in the genomes of virtually all small eukaryotic viruses but not in those of large eukaryotic viruses?. J Virol 1994;68:2889–2897[PubMed]
    [Google Scholar]
  12. Upadhyay M, Samal J, Kandpal M, Vasaikar S, Biswas B et al. CpG dinucleotide frequencies reveal the role of host methylation capabilities in parvovirus evolution. J Virol 2013;87:13816–13824 [CrossRef][PubMed]
    [Google Scholar]
  13. Shackelton LA, Parrish CR, Holmes EC. Evolutionary basis of codon usage and nucleotide composition bias in vertebrate DNA viruses. J Mol Evol 2006;62:551–563 [CrossRef][PubMed]
    [Google Scholar]
  14. Maeda K, Hondo E, Terakawa J, Kiso Y, Nakaichi N et al. Isolation of novel adenovirus from fruit bat (Pteropus dasymallus yayeyamae). Emerg Infect Dis 2008;14:347–349 [CrossRef][PubMed]
    [Google Scholar]
  15. Sonntag M, Mühldorfer K, Speck S, Wibbelt G, Kurth A. New adenovirus in bats, Germany. Emerg Infect Dis 2009;15:2052–2055 [CrossRef][PubMed]
    [Google Scholar]
  16. 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 [CrossRef][PubMed]
    [Google Scholar]
  17. 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 [CrossRef][PubMed]
    [Google Scholar]
  18. Baker KS, Leggett RM, Bexfield NH, Alston M, Daly G et al. Metagenomic study of the viruses of African straw-coloured fruit bats: detection of a chiropteran poxvirus and isolation of a novel adenovirus. Virology 2013;441:95–106 [CrossRef][PubMed]
    [Google Scholar]
  19. Tan B, Yang XL, Ge XY, Peng C, Zhang YZ et al. Novel bat adenoviruses with an extremely large E3 gene. J Gen Virol 2016;97:1625–1635 [CrossRef][PubMed]
    [Google Scholar]
  20. Hackenbrack N, Rogers MB, Ashley RE, Keel MK, Kubiski SV et al. Evolution and cryo-EM capsid structure of a North American bat adenovirus and its relationship to other mastadenoviruses. J Virol 2016
    [Google Scholar]
  21. Chen LH, Wu ZQ, Hu YF, Yang F, Yang J et al. [Genetic diversity of adenoviruses in bats of China]. Bing Du Xue Bao 2012;28:403–408 (in Chinese)[PubMed]
    [Google Scholar]
  22. Lima FE, Cibulski SP, Elesbao F, Carnieli Junior P, Batista HB et al. First detection of adenovirus in the vampire bat (Desmodus rotundus) in Brazil. Virus Genes 2013;47:378–381 [CrossRef][PubMed]
    [Google Scholar]
  23. 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 [CrossRef][PubMed]
    [Google Scholar]
  24. Anthony SJ, Epstein JH, Murray KA, Navarrete-Macias I, Zambrana-Torrelio CM et al. A strategy to estimate unknown viral diversity in mammals. MBio 2013;4:e00598–13 [CrossRef][PubMed]
    [Google Scholar]
  25. Casas I, Vazquez-Moron S, Juste J, Falcon A, Aznar C et al. Adenovirus Groups in Western Palaearctic Bats in Spain. GenBank Accession No: JX065117 to JX065129. 2010
  26. Zheng XY, Qiu M, Chen HF, Chen SW, Xiao JP et al. Molecular detection and phylogenetic characterization of bat and human adenoviruses in Southern China. Vector Borne Zoonotic Dis 2016;16:423–427 [CrossRef][PubMed]
    [Google Scholar]
  27. 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 [CrossRef][PubMed]
    [Google Scholar]
  28. 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 [CrossRef][PubMed]
    [Google Scholar]
  29. Farkas SL, Harrach B, Benko M. Completion of the genome analysis of snake adenovirus type 1, a representative of the reptilian lineage within the novel genus Atadenovirus. Virus Res 2008;132:132–139 [CrossRef][PubMed]
    [Google Scholar]
  30. To KK, Tse H, Chan WM, Choi GK, Zhang AJ et al. A novel psittacine adenovirus identified during an outbreak of avian chlamydiosis and human psittacosis: zoonosis associated with virus-bacterium coinfection in birds. PLoS Negl Trop Dis 2014;8:e3318 [CrossRef][PubMed]
    [Google Scholar]
  31. Hoelzer K, Shackelton LA, Parrish CR. Presence and role of cytosine methylation in DNA viruses of animals. Nucleic Acids Res 2008;36:2825–2837 [CrossRef][PubMed]
    [Google Scholar]
  32. Doerfler W. Epigenetic mechanisms in human adenovirus type 12 oncogenesis. Semin Cancer Biol 2009;19:136–143 [CrossRef][PubMed]
    [Google Scholar]
  33. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000;408:740–745 [CrossRef][PubMed]
    [Google Scholar]
  34. Krieg AM, Wu T, Weeratna R, Efler SM, Love-Homan L et al. Sequence motifs in adenoviral DNA block immune activation by stimulatory CpG motifs. Proc Natl Acad Sci USA 1998;95:12631–12636 [CrossRef][PubMed]
    [Google Scholar]
  35. Zhu J, Huang X, Yang Y. Innate immune response to adenoviral vectors is mediated by both Toll-like receptor-dependent and -independent pathways. J Virol 2007;81:3170–3180 [CrossRef][PubMed]
    [Google Scholar]
  36. Fejer G, Drechsel L, Liese J, Schleicher U, Ruzsics Z et al. Key role of splenic myeloid DCs in the IFN-αβ response to adenoviruses in vivo. PLoS Pathog 2008;4:e1000208 [CrossRef][PubMed]
    [Google Scholar]
  37. Kremer EJ, Nemerow GR. Adenovirus tales: from the cell surface to the nuclear pore complex. PLoS Pathog 2015;11:e1004821 [CrossRef][PubMed]
    [Google Scholar]
  38. Lee BL, Barton GM. Trafficking of endosomal Toll-like receptors. Trends Cell Biol 2014;24:360–369 [CrossRef][PubMed]
    [Google Scholar]
  39. Wuitschick JD, Karrer KM. Analysis of genomic G+C content, codon usage, initiator codon context and translation termination sites in Tetrahymena thermophila. J Eukaryot Microbiol 1999;46:239–247 [CrossRef][PubMed]
    [Google Scholar]
  40. Cui J, Schlub TE, Holmes EC. An allometric relationship between the genome length and virion volume of viruses. J Virol 2014;88:6403–6410 [CrossRef][PubMed]
    [Google Scholar]
  41. Guillén-Servent A, Francis CM. A new species of bat of the Hipposideros bicolor group (Chiroptera: hipposideridae) from Central Laos, with evidence of convergent evolution with Sundaic taxa. Acta Chiropterologica 2006;8:39–61 [CrossRef]
    [Google Scholar]
  42. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012;28:1647–1649 [CrossRef][PubMed]
    [Google Scholar]
  43. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. VISTA: computational tools for comparative genomics. Nucleic Acids Res 2004;32:W273–W279 [CrossRef][PubMed]
    [Google Scholar]
  44. Schorderet DF, Gartler SM. Analysis of CpG suppression in methylated and nonmethylated species. Proc Natl Acad Sci USA 1992;89:957–961 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000739
Loading
/content/journal/jgv/10.1099/jgv.0.000739
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error