Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes.

F Gao1 E Bailes D L Robertson Y Chen C M Rodenburg S F Michael L B Cummins L O Arthur M Peeters G M Shaw P M Sharp B H Hahn
Affiliations 1 institutions
  1. Department of Medicine, University of Alabama at Birmingham, 35294, USA.

Abstract

The human AIDS viruses human immunodeficiency virus type 1 (HIV-1) and type 2 (HIV-2) represent cross-species (zoonotic) infections. Although the primate reservoir of HIV-2 has been clearly identified as the sooty mangabey (Cercocebus atys), the origin of HIV-1 remains uncertain. Viruses related to HIV-1 have been isolated from the common chimpanzee (Pan troglodytes), but only three such SIVcpz infections have been documented, one of which involved a virus so divergent that it might represent a different primate lentiviral lineage. In a search for the HIV-1 reservoir, we have now sequenced the genome of a new SIVcpzstrain (SIVcpzUS) and have determined, by mitochondrial DNA analysis, the subspecies identity of all known SIVcpz-infected chimpanzees. We find that two chimpanzee subspecies in Africa, the central P. t. troglodytes and the eastern P. t. schweinfurthii, harbour SIVcpz and that their respective viruses form two highly divergent (but subspecies-specific) phylogenetic lineages. All HIV-1 strains known to infect man, including HIV-1 groups M, N and O, are closely related to just one of these SIVcpz lineages, that found in P. t. troglodytes. Moreover, we find that HIV-1 group N is a mosaic of SIVcpzUS- and HIV-1-related sequences, indicating an ancestral recombination event in a chimpanzee host. These results, together with the observation that the natural range of P. t. troglodytes coincides uniquely with areas of HIV-1 group M, N and O endemicity, indicate that P. t. troglodytes is the primary reservoir for HIV-1 and has been the source of at least three independent introductions of SIVcpz into the human population.

Supporting text Virus Host Location
Disease Reservoirs 149 Acquired Immunodeficiency Syndrome 3 Africa, Central 2 Africa, Eastern 1 Animals 1948 Ape Diseases 7 Chlorocebus aethiops 70 Disease Outbreaks 170 DNA, Mitochondrial 5 DNA, Viral 39 Evolution, Molecular 176 Female 289 Genome, Viral 317 HIV-1 11 Humans 1440 Meat 6 Molecular Sequence Data 160 Pan troglodytes 20 Phylogeny 805 Polymerase Chain Reaction 38 Recombination, Genetic 59 Sequence Alignment 51 Sequence Analysis, DNA 113 Simian Acquired Immunodeficiency Syndrome 10

Evidence records

6 total
Zoonotic Surveillance
3 records · 2 evidence types
Evidence type
2 records
OVE58
Key finding

SIVcpz viral RNA was detected in the central chimpanzee subspecies Pan troglodytes troglodytes in Africa.

Virus
Host
Location
Supporting text

We find that two chimpanzee subspecies in Africa, the central P. t. troglodytes ... harbour SIVcpz.

Method
sequencing | mitochondrial DNA analysis
Geographic raw
Africa
OVE59
Key finding

SIVcpz viral RNA was detected in the eastern chimpanzee subspecies Pan troglodytes schweinfurthii in Africa.

Virus
Host
Location
Supporting text

We find that two chimpanzee subspecies in Africa, the ... eastern P. t. schweinfurthii, harbour SIVcpz.

Method
sequencing | mitochondrial DNA analysis
Geographic raw
Africa
Evidence type
1 records
OVE62
Key finding

P. t. troglodytes was identified as the primary reservoir for HIV-1 based on subspecies-specific SIVcpz lineages and geographic overlap with HIV-1 endemicity.

Virus
Host
Location
Supporting text

These results, together with the observation that the natural range of P. t. troglodytes coincides uniquely with areas of HIV-1 group M, N and O endemicity, indicate that P. t. troglodytes is the primary reservoir for HIV-1

Method
sequenced the genome of a new SIVcpz strain | mitochondrial DNA analysis | phylogenetic analysis
Geographic raw
Africa | areas of HIV-1 group M, N and O endemicity
Genomic Evolution
3 records · 2 evidence types
Evidence type
1 records
OVE61
Key finding

HIV-1 group N is a mosaic of SIVcpzUS- and HIV-1-related sequences, indicating a recombination event that occurred in a chimpanzee host.

Virus
Host
Not specified
Location
Not specified
Supporting text

Moreover, we find that HIV-1 group N is a mosaic of SIVcpzUS- and HIV-1-related sequences, indicating an ancestral recombination event in a chimpanzee host.

Event type
recombination
Evidence type
2 records
OVE60
Key finding

SIVcpz viruses from Pan troglodytes troglodytes and Pan troglodytes schweinfurthii form two divergent subspecies-specific phylogenetic lineages, with human HIV-1 groups M, N, and O clustering closely with the P. t. troglodytes lineage.

Virus
Host
Location
Not specified
Supporting text

…their respective viruses form two highly divergent (but subspecies-specific) phylogenetic lineages. All HIV-1 strains known to infect man… are closely related to just one of these SIVcpz lineages, that found in P. t. troglodytes.

Analysis methods
phylogenetic analysis | sequence comparison
OVE63
Key finding

There have been at least three independent spillover events of SIVcpz from Pan troglodytes troglodytes into humans, giving rise to HIV-1 groups M, N, and O.

Virus
Host
Location
Not specified
Supporting text

…has been the source of at least three independent introductions of SIVcpz into the human population.

Analysis methods
genome sequencing | mitochondrial DNA analysis | phylogenetic comparison