1887

Journal of General Virology header logo

Volume 96, Issue 10

Phylogenomic evidence for recombination of adenoviruses in wild gorillas Free

Abstract

Human adenoviruses (HAdVs) of species (HAdV-B) are genetically highly diverse and comprise several pathogenic types. AdVs closely related to members of HAdV-B infect African great apes and the evolutionary origin of HAdV-B has recently been determined in ancient gorillas. Genetic evidence for intra- and inter-species recombination has been obtained for AdVs of humans and captive great apes, but evidence from wild great apes is lacking. In this study, potential HAdV-B members of wild Eastern gorillas were analysed for evidence of recombination. One near-complete genome was amplified from primary sample material and sequenced, and from another six individuals genome fragments were obtained. In phylogenomic analysis, their penton base, pVII–pVI, hexon and fiber genes were compared with those of all publicly available HAdV-B full-genome sequences of humans and captive great apes. Evidence for intra-species recombination between different HAdV-B members of wild gorillas as well as between HAdV-B members of chimpanzees and gorillas was obtained. Since zoonotic AdVs have been reported to cause respiratory outbreaks in both humans and monkeys, and humans in West and Central Africa frequently hunt and butcher primates thereby increasing the chance of zoonotic transmission, such HAdV-B recombinants might widen the pool of potential human pathogens.

  • Received:
  • Accepted:
  • Published Online:
© 2015 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000250
2015-10-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/10/3090.html?itemId=/content/journal/jgv/10.1099/jgv.0.000250&mimeType=html&fmt=ahah

References

  1. Abbink P., Lemckert A.A., Ewald B.A., Lynch D.M., Denholtz M., Smits S., Holterman L., Damen I., Vogels R., other authors. 2007; Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J Virol 81:4654–4663 [View Article][PubMed]
     [Google Scholar]
  2. Benson D.A., Cavanaugh M., Clark K., Karsch-Mizrachi I., Lipman D.J., Ostell J., Sayers E.W. 2013; GenBank. Nucleic Acids Res 14:(D1)D36–D42 [View Article][PubMed]
     [Google Scholar]
  3. Bray N., Dubchak I., Pachter L. 2003; Avid: a global alignment program. Genome Res 13:97–102 [View Article][PubMed]
     [Google Scholar]
  4. Chen E.C., Yagi S., Kelly K.R., Mendoza S.P., Tarara R.P., Canfield D.R., Maninger N., Rosenthal A., Spinner A., other authors. 2011; Cross-species transmission of a novel adenovirus associated with a fulminant pneumonia outbreak in a New World monkey colony. PLoS Pathog 7:e1002155 [View Article][PubMed]
     [Google Scholar]
  5. Chiu C.Y., Yagi S., Lu X., Yu G., Chen E.C., Liu M., Dick E.J. Jr, Carey K.D., Erdman D.D., other authors. 2013; A novel adenovirus species associated with an acute respiratory outbreak in a baboon colony and evidence of coincident human infection. MBio 4:e00084 [View Article][PubMed]
     [Google Scholar]
  6. Darriba D., Taboada G.L., Doallo R., Posada D. 2012; jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772 [View Article][PubMed]
     [Google Scholar]
  7. Dehghan S., Seto J., Jones M.S., Dyer D.W., Chodosh J., Seto D. 2013a; 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 447:265–273 [View Article][PubMed]
     [Google Scholar]
  8. Dehghan S., Seto J., Liu E.B., Walsh M.P., Dyer D.W., Chodosh J., Seto D. 2013b; Computational analysis of four human adenovirus type 4 genomes reveals molecular evolution through two interspecies recombination events. Virology 443:197–207 [View Article][PubMed]
     [Google Scholar]
  9. Duncan M., Cranfield M.R., Torano H., Kuete H.M., Lee G.P., Glenn A., Bruder J.T., Rangel D., Brough D.E., Gall J.G. 2013; Adenoviruses isolated from wild gorillas are closely related to human species C viruses. Virology 444:119–123 [View Article][PubMed]
     [Google Scholar]
  10. Ersching J., Hernandez M.I., Cezarotto F.S., Ferreira J.D., Martins A.B., Switzer W.M., Xiang Z., Ertl H.C., Zanetti C.R., Pinto A.R. 2010; Neutralizing antibodies to human and simian adenoviruses in humans and New-World monkeys. Virology 407:1–6 [View Article][PubMed]
     [Google Scholar]
  11. Frazer K.A., Pachter L., Poliakov A., Rubin E.M., Dubchak I. 2004; vista: computational tools for comparative genomics. Nucleic Acids Res 32:(Web Server)W273–W279 [View Article][PubMed]
     [Google Scholar]
  12. Guindon S., Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 [View Article][PubMed]
     [Google Scholar]
  13. Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. 2010; New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321 [View Article][PubMed]
     [Google Scholar]
  14. Hoppe E., Pauly M., Gillespie T.R., Akoua-Koffi C., Hohmann G., Fruth B., Karhemere S., Madinda N.F., Mugisha L., other authors. 2015; Multiple cross-species transmission events of human adenoviruses (HAdV) during hominine evolution. Mol Biol Evol 32:2072–2084 [View Article][PubMed]
     [Google Scholar]
  15. Kajon A.E., Lu X., Erdman D.D., Louie J., Schnurr D., George K.S., Koopmans M.P., Allibhai T., Metzgar D. 2010; Molecular epidemiology and brief history of emerging adenovirus 14-associated respiratory disease in the United States. J Infect Dis 202:93–103 [View Article][PubMed]
     [Google Scholar]
  16. Kandel R., Srinivasan A., D'Agata E.M.C., Lu X., Erdman D., Jhung M. 2010; Outbreak of adenovirus type 4 infection in a long-term care facility for the elderly. Infect Control Hosp Epidemiol 31:755–757 [View Article][PubMed]
     [Google Scholar]
  17. Kitamura N. 2001; Genome analysis of adenovirus type 7 and adenovirus type 11. Jpn J Ophthalmol 45:22–30 [View Article][PubMed]
     [Google Scholar]
  18. Lonsdorf E., Travis D., Ssuna R., Lantz E., Wilson M., Gamble K., Terio K., Leendertz F., Ehlers B., other authors. 2014; Field immobilization for treatment of an unknown illness in a wild chimpanzee (Pan troglodytes schweinfurthii) at Gombe National Park, Tanzania: findings, challenges, and lessons learned. Primates 55:89–99 [View Article][PubMed]
     [Google Scholar]
  19. Lukashev A.N., Ivanova O.E., Eremeeva T.P., Iggo R.D. 2008; Evidence of frequent recombination among human adenoviruses. J Gen Virol 89:380–388 [View Article][PubMed]
     [Google Scholar]
  20. Malhi Y., Adu-Bredu S., Asare R.A., Lewis S.L., Mayaux P. 2013; African rainforests: past, present and future. Philos Trans R Soc Lond B Biol Sci 368:20120312 [View Article][PubMed]
     [Google Scholar]
  21. Matsushima Y., Shimizu H., Kano A., Nakajima E., Ishimaru Y., Dey S.K., Watanabe Y., Adachi F., Mitani K., other authors. 2013; Genome sequence of a novel virus of the species human adenovirus d associated with acute gastroenteritis. Genome Announc 1:e00068 [View Article][PubMed]
     [Google Scholar]
  22. Mwenda J.M., Nyachieo A., Langat D.K., Steele D.A. 2005; Serological detection of adenoviruses in non-human primates maintained in a colony in Kenya. East Afr Med J 82:371–375[PubMed]
     [Google Scholar]
  23. Parrish C.R., Holmes E.C., Morens D.M., Park E.C., Burke D.S., Calisher C.H., Laughlin C.A., Saif L.J., Daszak P. 2008; Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol Mol Biol Rev 72:457–470 [View Article][PubMed]
     [Google Scholar]
  24. Pauly M., Hoppe E., Mugisha L., Petrzelkova K., Akoua-Koffi C., Couacy-Hymann E., Anoh A.E., Mossoun A., Schubert G., other authors. 2014; High prevalence and diversity of species D adenoviruses (HAdV-D) in human populations of four sub-Saharan countries. Virol J 11:25 [View Article][PubMed]
     [Google Scholar]
  25. Robinson C.M., Rajaiya J., Walsh M.P., Seto D., Dyer D.W., Jones M.S., Chodosh J. 2009; Computational analysis of human adenovirus type 22 provides evidence for recombination among species D human adenoviruses in the penton base gene. J Virol 83:8980–8985 [View Article][PubMed]
     [Google Scholar]
  26. Robinson C.M., Singh G., Lee J.Y., Dehghan S., Rajaiya J., Liu E.B., Yousuf M.A., Betensky R.A., Jones M.S., other authors. 2013a; Molecular evolution of human adenoviruses. Sci Rep 3:1812 [View Article][PubMed]
     [Google Scholar]
  27. Robinson C.M., Zhou X., Rajaiya J., Yousuf M.A., Singh G., DeSerres J.J., Walsh M.P., Wong S., Seto D., other authors. 2013b; Predicting the next eye pathogen: analysis of a novel adenovirus. MBio 4:e00595–e12 [View Article][PubMed]
     [Google Scholar]
  28. Roy S., Vandenberghe L.H., Kryazhimskiy S., Grant R., Calcedo R., Yuan X., Keough M., Sandhu A., Wang Q., other authors. 2009; Isolation and characterization of adenoviruses persistently shed from the gastrointestinal tract of non-human primates. PLoS Pathog 5:e1000503 [View Article][PubMed]
     [Google Scholar]
  29. Ryan M.A., Gray G.C., Smith B., McKeehan J.A., Hawksworth A.W., Malasig M.D. 2002; Large epidemic of respiratory illness due to adenovirus types 7 and 3 in healthy young adults. Clin Infect Dis 34:577–582 [View Article][PubMed]
     [Google Scholar]
  30. Sanchez J.L., Binn L.N., Innis B.L., Reynolds R.D., Lee T., Mitchell-Raymundo F., Craig S.C., Marquez J.P., Shepherd G.A., other authors. 2001; Epidemic of adenovirus-induced respiratory illness among US military recruits: epidemiologic and immunologic risk factors in healthy, young adults. J Med Virol 65:710–718 [View Article][PubMed]
     [Google Scholar]
  31. Seimon T.A., Olson S.H., Lee K.J., Rosen G., Ondzie A., Cameron K., Reed P., Anthony S.J., Joly D.O., other authors. 2015; Adenovirus and herpesvirus diversity in free-ranging great apes in the Sangha region of the Republic of Congo. PLoS One 10:e0118543 [View Article][PubMed]
     [Google Scholar]
  32. Tang L., Wang L., Tan X., Xu W. 2011; Adenovirus serotype 7 associated with a severe lower respiratory tract disease outbreak in infants in Shaanxi Province, China. Virol J 8:23 [View Article][PubMed]
     [Google Scholar]
  33. Tate J.E., Bunning M.L., Lott L., Lu X., Su J., Metzgar D., Brosch L., Panozzo C.A., Marconi V.C., other authors. 2009; Outbreak of severe respiratory disease associated with emergent human adenovirus serotype 14 at a US air force training facility in 2007. J Infect Dis 199:1419–1426 [View Article][PubMed]
     [Google Scholar]
  34. Wadell G. 1984; Molecular epidemiology of human adenoviruses. Curr Top Microbiol Immunol 110:191–220[PubMed]
     [Google Scholar]
  35. Walsh M.P., Chintakuntlawar A., Robinson C.M., Madisch I., Harrach B., Hudson N.R., Schnurr D., Heim A., Chodosh J., other authors. 2009; Evidence of molecular evolution driven by recombination events influencing tropism in a novel human adenovirus that causes epidemic keratoconjunctivitis. PLoS One 4:e5635 [View Article][PubMed]
     [Google Scholar]
  36. Wevers D., Leendertz F.H., Scuda N., Boesch C., Robbins M.M., Head J., Ludwig C., Kühn J., Ehlers B. 2010; A novel adenovirus of Western lowland gorillas (Gorilla gorilla gorilla). Virol J 7:303 [View Article][PubMed]
     [Google Scholar]
  37. Wevers D., Metzger S., Babweteera F., Bieberbach M., Boesch C., Cameron K., Couacy-Hymann E., Cranfield M., Gray M., other authors. 2011; Novel adenoviruses in wild primates: a high level of genetic diversity and evidence of zoonotic transmissions. J Virol 85:10774–10784 [View Article][PubMed]
     [Google Scholar]
  38. Woolhouse M., Gaunt E. 2007; Ecological origins of novel human pathogens. Crit Rev Microbiol 33:231–242 [View Article][PubMed]
     [Google Scholar]
  39. Xiang Z., Li Y., Cun A., Yang W., Ellenberg S., Switzer W.M., Kalish M.L., Ertl H.C. 2006; Chimpanzee adenovirus antibodies in humans, sub-Saharan Africa. Emerg Infect Dis 12:1596–1599 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000250
Loading
Phylogenomic evidence for recombination of adenoviruses in wild gorillas
J. Gen. Virol. 96, 3090 (2015); https://doi.org/10.1099/jgv.0.000250
/content/journal/jgv/10.1099/jgv.0.000250
/content/journal/jgv/10.1099/jgv.0.000250
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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