Origin of the HIV-1 group O epidemic in western lowland gorillas.
HIV-1, the cause of AIDS, is composed of four phylogenetic lineages, groups M, N, O, and P, each of which resulted from an independent cross-species transmission event of simian immunodeficiency viruses (SIVs) infecting African apes. Although groups M and N have been traced to geographically distinct chimpanzee communities in southern Cameroon, the reservoirs of groups O and P remain unknown. Here, we screened fecal samples from western lowland (n = 2,611), eastern lowland (n = 103), and mountain (n = 218) gorillas for gorilla SIV (SIVgor) antibodies and nucleic acids. Despite testing wild troops throughout southern Cameroon (n = 14), northern Gabon (n = 16), the Democratic Republic of Congo (n = 2), and Uganda (n = 1), SIVgor was identified at only four sites in southern Cameroon, with prevalences ranging from 0.8-22%. Amplification of partial and full-length SIVgor sequences revealed extensive genetic diversity, but all SIVgor strains were derived from a single lineage within the chimpanzee SIV (SIVcpz) radiation. Two fully sequenced gorilla viruses from southwestern Cameroon were very closely related to, and likely represent the source population of, HIV-1 group P. Most of the genome of a third SIVgor strain, from central Cameroon, was very closely related to HIV-1 group O, again pointing to gorillas as the immediate source. Functional analyses identified the cytidine deaminase APOBEC3G as a barrier for chimpanzee-to-gorilla, but not gorilla-to-human, virus transmission. These data indicate that HIV-1 group O, which spreads epidemically in west central Africa and is estimated to have infected around 100,000 people, originated by cross-species transmission from western lowland gorillas.
Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France; Laboratory of Human Virology, Universidade Federal do Rio de Janeiro, 21949-570 Rio de Janeiro, Brazil;
Mirela
M
D'arc
Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France;
Ahidjo
A
Ayouba
Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France;
Amandine
A
Esteban
Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104;
Gerald H
GH
Learn
Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France; Centre International de Recherches Médicales, Franceville, Gabon;
Vanina
V
Boué
Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France; Centre International de Recherches Médicales, Franceville, Gabon;
Florian
F
Liegeois
Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France;
Lucie
L
Etienne
Projet Grands Singes, Center for Research and Conservation, Royal Zoological Society of Antwerp, 2018 Antwerp, Belgium;
Nikki
N
Tagg
Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, 13353 Berlin, Germany;
Fabian H
FH
Leendertz
Department of Primatology, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany;
Christophe
C
Boesch
Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, 13353 Berlin, Germany; Department of Primatology, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany; Institut de Recherche en Ecologie Tropicale, Libreville, Gabon;
Nadège F
NF
Madinda
Department of Primatology, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany;
Martha M
MM
Robbins
International Gorilla Conservation Programme, Kigali, Rwanda;
Maryke
M
Gray
Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France;
Amandine
A
Cournil
Department of Microbiology, Global Health and Emerging Pathogens Institute, and.
Marcel
M
Ooms
Department of Microbiology, Global Health and Emerging Pathogens Institute, and.
Michael
M
Letko
Department of Microbiology, Global Health and Emerging Pathogens Institute, and Division of Infectious Diseases, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029;
Viviana A
VA
Simon
Institute of Evolutionary Biology, and Center for Immunity, Infection, and Evolution, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom;
Paul M
PM
Sharp
Departments of Medicine and Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104; bhahn@upenn.edu martine.peeters@ird.fr.
Beatrice H
BH
Hahn
Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France;
Eric
E
Delaporte
Institut de Recherches Médicales et d'Études des Plantes Médicinales, Prévention du Sida au Cameroun, Yaoundé, Cameroon; and.
Eitel
E
Mpoudi Ngole
Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, 34394 Montpellier, France; Computational Biology Institute, 34095 Montpellier, France bhahn@upenn.edu martine.peeters@ird.fr.
Martine
M
Peeters
D000818:Animals; D000835:Animals, Wild / Q000821:virology; D000914:Antibodies, Viral / Q000276:immunology; D005075:Biological Evolution; D002163:Cameroon / Q000453:epidemiology; D003564:Cytidine Deaminase / Q000378:metabolism; D058872:Epidemics; D005243:Feces / Q000821:virology; D014644:Genetic Variation; D016678:Genome / Q000235:genetics; D005843:Geography; D006071:Gorilla gorilla / Q000821:virology*; D015497:HIV-1 / Q000502:physiology*; D006801:Humans; D008969:Molecular Sequence Data; D010802:Phylogeny; D059748:Proteolysis; D017422:Sequence Analysis, DNA; D016097:Simian Acquired Immunodeficiency Syndrome / Q000453:epidemiology* / Q000276:immunology / Q000821:virology*; D015302:Simian Immunodeficiency Virus / Q000276:immunology
D000914:Antibodies, Viral; D003564:Cytidine Deaminase
AIDS; HIV-1; SIVgor; gorilla; zoonotic transmission