Multiple Cross-Species Transmission Events of Human Adenoviruses (HAdV) during Hominine Evolution
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
25862141
PubMed Central
PMC4833075
DOI
10.1093/molbev/msv090
PII: msv090
Knihovny.cz E-zdroje
- Klíčová slova
- African great apes, adenovirus, zoonosis,
- MeSH
- Adenoviridae * genetika patogenita MeSH
- adenovirové infekce * genetika přenos MeSH
- druhová specificita MeSH
- Hominidae virologie MeSH
- lidé MeSH
- molekulární evoluce * MeSH
- zoonózy genetika přenos MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Human adenoviruses (HAdV; species HAdV-A to -G) are highly prevalent in the human population, and represent an important cause of morbidity and, to a lesser extent, mortality. Recent studies have identified close relatives of these viruses in African great apes, suggesting that some HAdV may be of zoonotic origin. We analyzed more than 800 fecal samples from wild African great apes and humans to further investigate the evolutionary history and zoonotic potential of hominine HAdV. HAdV-B and -E were frequently detected in wild gorillas (55%) and chimpanzees (25%), respectively. Bayesian ancestral host reconstruction under discrete diffusion models supported a gorilla and chimpanzee origin for these viral species. Host switches were relatively rare along HAdV evolution, with about ten events recorded in 4.5 My. Despite presumably rare direct contact between sympatric populations of the two species, transmission events from gorillas to chimpanzees were observed, suggesting that habitat and dietary overlap may lead to fecal-oral cross-hominine transmission of HAdV. Finally, we determined that two independent HAdV-B transmission events to humans occurred more than 100,000 years ago. We conclude that HAdV-B circulating in humans are of zoonotic origin and have probably affected global human health for most of our species lifetime.
Department of Primatology Max Planck Institute for Evolutionary Anthropology Leipzig Germany
Epidemiology of highly pathogenic microorganisms Robert Koch Institute Berlin Germany
Institut National de Recherche Biomédicale Kinshasa Democratic Republic of Congo
International Gorilla Conservation Program Kigali Rwanda
North Carolina Zoological Park Asheboro NC
World Wildlife Foundation Dzanga Sangha Protected Areas Bangui Central African Republic
Zobrazit více v PubMed
Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol. 2012;29:2157–2167. PubMed PMC
Betsem E, Rua R, Tortevoye P, Froment A, Gessain A. Frequent and recent human acquisition of simian foamy viruses through apes' bites in central Africa. PLoS Pathog. 2011;7:e1002306. PubMed PMC
Calvignac-Spencer S, Leendertz SA, Gillespie TR, Leendertz FH. Wild great apes as sentinels and sources of infectious disease. Clin Microbiol Infect. 2012;18:521–527. PubMed
Chen EC, Yagi S, Kelly KR, Mendoza SP, Tarara RP, Canfield DR, Maninger N, Rosenthal A, Spinner A, Bales KL, 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. PubMed PMC
Chiu CY, Yagi S, Lu X, Yu G, Chen EC, Liu M, Dick EJ, Jr, Carey KD, Erdman DD, Leland MM, et al. A novel adenovirus species associated with an acute respiratory outbreak in a baboon colony and evidence of coincident human infection. MBio. 2013;4:e00084. PubMed PMC
Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9:772–772. PubMed PMC
Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29:1969–1973. PubMed PMC
Duffy S, Shackelton LA, Holmes EC. Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet. 2008;9:267–276. PubMed
Duval L, Fourment M, Nerrienet E, Rousset D, Sadeuh SA, Goodman SM, Andriaholinirina NV, Randrianarivelojosia M, Paul RE, Robert V, et al. African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus. Proc Natl Acad Sci U S A. 2010;107:10561–10566. PubMed PMC
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. PubMed PMC
Ersching J, Hernandez MI, Cezarotto FS, Ferreira JD, Martins AB, Switzer WM, Xiang Z, Ertl HC, Zanetti CR, Pinto AR. Neutralizing antibodies to human and simian adenoviruses in humans and New-World monkeys. Virology. 2010;407:1–6. PubMed
Fourment M, Gibbs MJ. PATRISTIC: a program for calculating patristic distances and graphically comparing the components of genetic change. BMC Evol Biol. 2006;6:1. PubMed PMC
Fujisawa T, Barraclough TG. Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Syst Biol. 2013;62:707–724. PubMed PMC
Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27:221–224. PubMed
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–321. PubMed
Guindon S, Lethiec F, Duroux P, Gascuel O. PHYML Online-a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 2005;33:W557–W559. PubMed PMC
Harrach B, Benkö M, Both GW, Brown M, Davison AJ, Echavarria M, Hess M, Jones MS, Kajon A, Lehmkuhl HD, 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.
Hasegawa H, Modry D, Kitagawa M, Shutt KA, Todd A, Kalousova B, Profousova I, Petrzelkova KJ. Humans and great apes cohabiting the forest ecosystem in central african republic harbour the same hookworms. PLoS Negl Trop Dis. 2014;8:e2715. PubMed PMC
Head J, Boesch C, Makaga L, Robbins M. Sympatric chimpanzees (Pan troglodytes troglodytes) and gorillas (Gorilla gorilla gorilla) in Loango National Park, Gabon: dietary composition, seasonality, and intersite comparisons. Int J Primatol. 2011;32:755–775.
Heled J, Drummond AJ. Bayesian inference of species trees from multilocus data. Mol Biol Evol. 2010;27:570–580. PubMed PMC
Junker J, Blake S, Boesch C, Campbell G, Toit LD, Duvall C, Ekobo A, Etoga G, Galat-Luong A, Gamys J, et al. Recent decline in suitable environmental conditions for African great apes. Divers Distrib. 2012;18:1077–1091.
Kaiser M, Lowa A, Ulrich M, Ellerbrok H, Goffe AS, Blasse A, Zommers Z, Couacy-Hymann E, Babweteera F, Zuberbuhler K, et al. Wild chimpanzees infected with 5 Plasmodium species. Emerg Infect Dis. 2010;16:1956–1959. PubMed PMC
Kajon AE, Lu X, Erdman DD, Louie J, Schnurr D, George KS, Koopmans MP, Allibhai T, Metzgar D. Molecular epidemiology and brief history of emerging adenovirus 14-associated respiratory disease in the United States. J Infect Dis. 2010;202:93–103. PubMed
Keele BF, Van Heuverswyn F, Li Y, Bailes E, Takehisa J, Santiago ML, Bibollet-Ruche F, Chen Y, Wain LV, Liegeois F, et al. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science. 2006;313:523–526. PubMed PMC
Kent RJ. Molecular methods for arthropod bloodmeal identification and applications to ecological and vector-borne disease studies. Mol Ecol Resour. 2009;9:4–18. PubMed
Krief S, Escalante AA, Pacheco MA, Mugisha L, Andre C, Halbwax M, Fischer A, Krief JM, Kasenene JM, Crandfield M, et al. On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from Bonobos. PLoS Pathog. 2010;6:e1000765. PubMed PMC
Lemey P, Rambaut A, Drummond AJ, Suchard MA. Bayesian phylogeography finds its roots. PLoS Comput Biol. 2009;5:e1000520. PubMed PMC
Lion T. Adenovirus Infections in Immunocompetent and Immunocompromised Patients. Clin Microbiol Rev. 2014;27:441–462. PubMed PMC
Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, Ndjango JB, Sanz CM, Morgan DB, Locatelli S, et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature. 2010;467:420–425. PubMed PMC
Malhi Y, Adu-Bredu S, Asare RA, Lewis SL, Mayaux P. African rainforests: past, present and future. Philos Trans R Soc Lond B Biol Sci. 2013;368:20120312. PubMed PMC
Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P. RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics. 2010;26:2462–2463. PubMed PMC
McDougall I, Brown FH, Fleagle JG. Stratigraphic placement and age of modern humans from Kibish, Ethiopia. Nature. 2005;433:733–736. PubMed
Minin VN, Suchard MA. Fast, accurate and simulation-free stochastic mapping. Philos Trans R Soc Lond B Biol Sci. 2008;363:3985–3995. PubMed PMC
Mwenda JM, Nyachieo A, Langat DK, Steele DA. Serological detection of adenoviruses in non-human primates maintained in a colony in Kenya. East Afr Med J. 2005;82:371–375. PubMed
Neel C, Etienne L, Li Y, Takehisa J, Rudicell RS, Bass IN, Moudindo J, Mebenga A, Esteban A, Van Heuverswyn F, et al. Molecular epidemiology of simian immunodeficiency virus infection in wild-living gorillas. J Virol. 2010;84:1464–1476. PubMed PMC
Oelze VM, Head JS, Robbins MM, Richards M, Boesch C. Niche differentiation and dietary seasonality among sympatric gorillas and chimpanzees in Loango National Park (Gabon) revealed by stable isotope analysis. J Hum Evol. 2014;66:95–106. PubMed
Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol. 2006;55:595–609. PubMed
Prado-Martinez J, Sudmant PH, Kidd JM, Li H, Kelley JL, Lorente-Galdos B, Veeramah KR, Woerner AE, O'Connor TD, Santpere G, et al. Great ape genetic diversity and population history. Nature. 2013;499:471–475. PubMed PMC
Prugnolle F, Durand P, Neel C, Ollomo B, Ayala FJ, Arnathau C, Etienne L, Mpoudi-Ngole E, Nkoghe D, Leroy E, et al. African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proc Natl Acad Sci U S A. 2010;107:1458–1463. PubMed PMC
Prugnolle F, Rougeron V, Becquart P, Berry A, Makanga B, Rahola N, Arnathau C, Ngoubangoye B, Menard S, Willaume E, et al. Diversity, host switching and evolution of Plasmodium vivax infecting African great apes. Proc Natl Acad Sci U S A. 2013;110:8123–8128. PubMed PMC
Purkayastha A, Ditty SE, Su J, McGraw J, Hadfield TL, Tibbetts C, Seto D. 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. PubMed PMC
Rayner JC, Liu W, Peeters M, Sharp PM, Hahn BH. A plethora of Plasmodium species in wild apes: a source of human infection? Trends Parasitol. 2011;27:222–229. PubMed PMC
Roy S, Gao G, Clawson DS, Vandenberghe LH, Farina SF, Wilson JM. Complete nucleotide sequences and genome organization of four chimpanzee adenoviruses. Virology. 2004;324:361–372. PubMed
Roy S, Vandenberghe LH, Kryazhimskiy S, Grant R, Calcedo R, Yuan X, Keough M, Sandhu A, Wang Q, Medina-Jaszek CA, et al. Isolation and characterization of adenoviruses persistently shed from the gastrointestinal tract of non-human primates. PLoS Pathog. 2009;5:e1000503. PubMed PMC
Rwego IB, Isabirye-Basuta G, Gillespie TR, Goldberg TL. Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conserv Biol. 2008;22:1600–1607. PubMed
Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I, Herrero J, Hobolth A, Lappalainen T, Mailund T, Marques-Bonet T, et al. Insights into hominid evolution from the gorilla genome sequence. Nature. 2012;483:169–175. PubMed PMC
Sharp PM, Hahn BH. Origins of HIV and the AIDS pandemic. Cold Spring Harb Perspect Med. 2011;1:a006841. PubMed PMC
Sundararaman SA, Liu W, Keele BF, Learn GH, Bittinger K, Mouacha F, Ahuka-Mundeke S, Manske M, Sherrill-Mix S, Li Y, et al. Plasmodium falciparum-like parasites infecting wild apes in southern Cameroon do not represent a recurrent source of human malaria. Proc Natl Acad Sci U S A. 2013;110:7020–7025. PubMed PMC
Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56:564–577. PubMed
Van Heuverswyn F, Li Y, Neel C, Bailes E, Keele BF, Liu W, Loul S, Butel C, Liegeois F, Bienvenue Y, et al. Human immunodeficiency viruses: SIV infection in wild gorillas. Nature. 2006;444:164. PubMed
Verhulst NO, Smallegange RC, Takken W. Mosquitoes as potential bridge vectors of malaria parasites from non-human primates to humans. Front Physiol. 2012;3:197. PubMed PMC
Villesen P. FaBox: an online toolbox for fasta sequences. Mol Ecol Notes. 2007;7:965–968.
Walsh PD, Breuer T, Sanz C, Morgan D, Doran-Sheehy D. Potential for Ebola transmission between gorilla and chimpanzee social groups. Am Nat. 2007;169:684–689. PubMed
Weinert LA, Welch JJ, Suchard MA, Lemey P, Rambaut A, Fitzgerald JR. Molecular dating of human-to-bovid host jumps by Staphylococcus aureus reveals an association with the spread of domestication. Biol Lett. 2012;8:829–832. PubMed PMC
Wevers D, Leendertz FH, Scuda N, Boesch C, Robbins MM, Head J, Ludwig C, Kuhn J, Ehlers B. A novel adenovirus of Western lowland gorillas (Gorilla gorilla gorilla) Virol J. 2010;7:303. PubMed PMC
Wevers D, Metzger S, Babweteera F, Bieberbach M, Boesch C, Cameron K, Couacy-Hymann E, Cranfield M, Gray M, Harris LA, et al. Novel adenoviruses in wild primates: a high level of genetic diversity and evidence of zoonotic transmissions. J Virol. 2011;85:10774–10784. PubMed PMC
Xiang Z, Li Y, Cun A, Yang W, Ellenberg S, Switzer WM, Kalish ML, Ertl HC. Chimpanzee adenovirus antibodies in humans, sub-Saharan Africa. Emerg Infect Dis. 2006;12:1596–1599. PubMed PMC
Yamagiwa J, Basabose AK. Diet and seasonal changes in sympatric gorillas and chimpanzees at Kahuzi-Biega National Park. Primates. 2006;47:74–90. PubMed
Yamagiwa J, Basabose AK. Fallback foods and dietary partitioning among Pan and Gorilla. Am J Phys Anthropol. 2009;140:739–750. PubMed