Chimpanzee reservoirs of pandemic and nonpandemic HIV-1

Abstract

Human immunodeficiency virus type 1 (HIV-1), the cause of human acquired immunodeficiency syndrome (AIDS), is a zoonotic infection of staggering proportions and social impact. Yet uncertainty persists regarding its natural reservoir. The virus most closely related to HIV-1 is a simian immunodeficiency virus (SIV) thus far identified only in captive members of the chimpanzee subspecies Pan troglodytes troglodytes. Here we report the detection of SIVcpz antibodies and nucleic acids in fecal samples from wild-living P. t. troglodytes apes in southern Cameroon, where prevalence rates in some communities reached 29 to 35%. By sequence analysis of endemic SIVcpz strains, we could trace the origins of pandemic (group M) and nonpandemic (group N) HIV-1 to distinct, geographically isolated chimpanzee communities. These findings establish P. t. troglodytes as a natural reservoir of HIV-1.

Figures

Fig. 1

Natural ranges of the four chimpanzee subspecies (top) and locations of wild chimpanzee study sites WE, MT, DG, DP, BQ, EK, CP, BB, MB, and LB in southern Cameroon (inset and bottom). Field sites with endemic SIVcpzPtt infection are color-coded to correspond with the SIVcpzPtt lineages shown in Figs. 3 and 4.

Fig. 2

Detection of SIVcpz antibodies in chimpanzee fecal samples. Fecal samples from wild-living chimpanzees were tested by enhanced chemiluminescent Western blot using HIV-1 antigen–containing strips. Samples are numbered, with letters indicating their collection site as shown in Fig. 1. Samples from the same individual (ID) are grouped. Asterisks indicate two antibody-negative but virion RNA–positive samples (also see table S3). Molecular weights of HIV-1 proteins are indicated. The banding patterns of plasma from HIV-1–infected (Pos) and –uninfected (Neg) humans are shown as controls.

Fig. 3

Phylogenetic analysis of SIVcpzPtt strains from wild P. t. troglodytes apes. Newly identified SIVcpzPtt strains are highlighted by colors reflecting their collection sites (Fig. 1). Representative strains of HIV-1 groups M, N, and O and SIVcpzPts (TAN1, TAN2, TAN3, and ANT) are shown. Trees were inferred by the Bayesian method; numbers on nodes are percentage posterior probabilities (only values above 95% are shown). The scale bars represent 0.05 and 0.1 substitutions per site. Pol, polymerase; gp41, envelope transmembrane protein.

Fig. 4

Evolutionary relationships of SIVcpz and HIV-1 strains based on full-length sequences. Trees were inferred by the Bayesian method for Gag, Pol, and Env; the Pol protein was separated into two fragments at a recombination breakpoint previously identified in HIV-1 group N (5, 21); the C terminus of Pol was concatenated with downstream Vif sequences. Sequences are color-coded as in Fig. 3. Numbers on internal branches indicate estimated posterior probabilities (only values above 95% are shown). The scale bars represent 0.05 and 0.1 substitutions per site. Arrows indicate branches where cross-species transmissions gave rise to HIV-1 groups M and N.