Genetic diversity of STLV-2 and interspecies transmission of STLV-3 in wild-living bonobos

Abstract

There are currently four known primate T-cell lymphotropic virus groups (PTLV1-4), each of which comprises closely related simian (STLV) and human (HTLV) viruses. For PTLV-1 and PTLV-3, simian and human viruses are interspersed, suggesting multiple cross-species transmission events; however, for PTLV-2 this is not so clear because HTLV-2 and STLV-2 strains from captive bonobos (Pan paniscus) form two distinct clades. To determine to what extent bonobos are naturally infected with STLV, we screened fecal samples (n = 633) from wild-living bonobos (n = 312) at six different sites in the Democratic Republic of Congo (DRC) for the presence of STLV nucleic acids. STLV infection was detected in 8 of 312 bonobos at four of six field sites, suggesting an overall prevalence of 2.6% (ranging from 0 to 8%). Six samples contained STLV-2, while the two others contained STLV-3, as determined by phylogenetic analysis of partial tax and Long Terminal Repeats (LTR) sequences. The new STLV-2 sequences were highly diverse, but grouped with previously identified STLV-2 strains as a sister clade to HTLV-2. In contrast, the new STLV-3 sequences did not cluster together, but were more closely related to STLVs from sympatric monkey species. These results show for the first time that fecal samples can be used to detect STLV infection in apes. These results also show that wild-living bonobos are endemically infected with STLV-2, but have acquired STLV-3 on at least two occasions most likely by cross-species transmission from monkey species on which they prey. Future studies of bonobos and other non-human primate species in Central Africa are needed to identify the simian precursor of HTLV-2 in humans.

Keywords: DRC; STLV-2; STLV-3; bonobos; feces.

Figure 1.

Distribution area of African great apes and the bonobo (Pan paniscus) range (in red) in DRC are depicted. The location of bonobo fecal sample collection sites in DRC are indicated with circles and a two-letter code: BN, Balanga; IK, Ikela; KR, Kokolopori; LK, Lui-kotal, ML, Malebo and LA, Lomako-Yokokala . Rwanda (Rw) and Burundi (Bu) are indicated with the first two letters of the country’s name.

Figure 2.

Mid-point rooted PTLVphylogeny inferred from 202-bp tax sequences. The tree was generated using ML methods, with the TN93 nucleotide substitution model with gamma-distributed rates among sites. Numbers correspond to internal branch support derived from 100 bootstrap replicates. Scale bar represents the number of nucleotide substitutions per site. The different PTLV types are indicated. New PTLV-1 sequences are highlighted in dotted red lines boxes, strains isolated in humans are highlighted in blue font. STLV sequences from the DRC are highlighted in green. Different NHP species are indicated with the following abbreviations; Pth, Piliocolobus tholloni; Cas, Cercopithecus ascanius; Cwo, Cercopithecus wolfi; Cni, Cercopithecus nictitans; Cpo, Cercopithecus pogonias; Cce, Cercopithecus cephus; Cne, Cercopithecus neglectus; Lat, Lophocebus atterrimus; Lal, Lophocebus albigena; Can, Colobus angolensis; Cag, Cercocebus agilis; Pha, Papio hamadryas; Ggo, Gorilla gorilla.

Figure 3.

Mid-point rooted PTLV-2 phylogeny inferred from 313-bp LTR sequences. The tree was generated using ML methods with the TN93 nucleotide substitution model with gamma-distributed rates among sites. Numbers correspond to internal branch support derived from 100 bootstrap replicates. Scale bar represents the number of nucleotide substitutions per site. The new STLV-2 sequence is highlighted in dotted red line box. Human-derived strains are highlighted in blue font.

Figure 4.

Mid-point rooted PTLV-3 phylogeny inferred from 380-bp LTR sequences. The tree was inferred using ML methods with the TN93 nucleotide substitution model with gamma-distributed rates among sites. Numbers correspond to internal branch support derived from 100 bootstrap replicates. Scale bar represents the number of nucleotide substitutions per site. The different PTLV-3 subtypes are indicated. The new STLV-3 sequence is highlighted in green box. STLV-3 and HTLV-3 sequences are highlighted in colors according to their geographic origin, green for DRC, black from Cameroon, orange for Gabon, magenta for Senegal and grey for Ehtiopia/Eritrea. Different NHP species are indicated with the following abbreviations; Cag, Cercocebus agilis; Cto, Cercocebus torquatus; Lat, Lophocebus atterrimus; Can, Colobus angolensis; Lal, Lophocebus albigena; Pth, Piliocolobus tholloni; Cni, Cercopithecus nictitans; Cmo, Cercopithecus mona; Ph, Papio hamadryas; Ppa, Papio anubis; Tge, Theropithecus gelada. HTLV-3 strains are highlighted in blue font.