Novel gamma-1 herpesviruses identified in free-ranging new world monkeys (golden-handed tamarin [Saguinus midas], squirrel monkey [Saimiri sciureus], and white-faced saki [Pithecia pithecia]) in French Guiana

Abstract

The recent finding of a novel Epstein-Barr virus-related lymphocryptovirus (CalHV-3) in a captive colony of common marmoset (Callithrix jacchus) in the United States modifies the view that the host range of lymphocryptovirus is restricted to humans and Old World primates. We investigated the presence of Epstein-Barr virus-related viruses in 79 samples of New World monkeys caught in the wild, including six species of the Cebidae family and one of the Callitrichidae, living in the rain forest of French Guiana. Using a degenerate consensus PCR method for the herpesvirus DNA polymerase gene, we identified three novel lymphocryptoviruses from golden-handed tamarin (Saguinus midas) of the Callitrichidae family and squirrel monkey (Saimiri sciureus) and white-faced saki (Pithecia pithecia) of the Cebidae family. With the CalHV-3 strain, these three novel viruses constitute a well-supported phylogenetic clade in the Lymphocryptovirus genus, which is clearly distinct from the lineage of Old World lymphocryptovirus, hosted by catarrhine monkeys and humans. In tamarins, the prevalence of the novel lymphocryptovirus was more than 50%, indicating that it circulates well in the wild population, perhaps due to specific ecoethological patterns such as confrontations and intergroup migration. The detection and partial molecular characterization of the polymerase gene of three novel Gamma-1-Herpesvirinae from New World monkeys caught in the wild clearly indicate that free-ranging populations of platyrrhine are natural hosts of lymphocryptoviruses. Further characterization of these novel viruses will provide new insight not only into the origin and evolution of Gammaherpesvirinae but also into their pathogenicity.

FIG. 1.

Phylogenetic tree resulting from analysis of selected 426-bp fragments of herpesvirus DNA polymerase gene (primers QAHNA and GDTD1B) (26), which is available for all viruses. The phylogeny was derived by the neighbor-joining method applied to pairwise sequence distances calculated by the Kimura two-parameter method (transition-to-transversion ratio set at 2). Horizontal branch lengths are drawn to scale, with the bar indicating 0.1 nucleotide replacements per site. Numbers at each node indicate the percentage of bootstrap samples (out of 100) in which the cluster to the right is supported. Brackets on the right indicate previously defined subfamily and genus herpesviral classification. Previously published sequences included and their accession numbers are as follows: HSV1 (X04771); HSV2 (M16321); VZV (X04370); EBV (V01555); HCMV (M14709); HHV6A (X83413); HHV7 (U43400); KSHV (U75698, U93872 and AF005477); H. saimiri HVS (M31122); HVA3 (AF083424); ChRV1 (AJ251573); ChRV2 (AJ251574); RFHVMn (AF005478); RFHVMm (AF005479); RRV/17577 (AF083501); RRV/H26-95 (AF029302); MneRV2 (AF204167); Macaca gamma virus strains from Macaca mulatta (AF159033), Macaca fascicularis (AF159032), and Macaca nemestrina (AF159031), called here MGVMm, MGVMf and MGVMn, respectively; PanRHV1a (AF250879 and AF250880); PanRHV1b(AF250881 and AF250882); PanRHV2 (AF346490); GorRHV1 (AF250886); MndRHV1 (AF282943); MndRHV2 (AF282937 to AF282940); Cercopithecine hv15 (AY037858); CalHV-3 (AF319782); MndHVβ (AF282942); PRV (L24487); BHV1 (Z78205); EHV1 (M86664); GHV2 (L40431); MCMV (U68299); RhCMV (AF0033184); MndCMV (AF282941); baboon CMV (AF27664); vervet CMV (AY049066); Cercopithecine hv3 (AY049065); chimpanzee CMV (AF480884); cebus CMV (AF292067); S. sciureus CMV (AF292065); MHV68 (U97553); BHV4 (AF031811); EHV2 (U20824); BLHV (AF031808); AHV1 (AF005370); and OHV2 (AF031812).

FIG. 2.

Neighbor-joining protein distance tree for the 142 amino acid residues encoded by the 426-bp fragment (primers QAHNA and GDTD1B) (26) of DNA polymerase. Sequences were aligned by ClustalW and were analyzed with the PROTDIST and NEIGHBOR programs in PHYLIP. One hundred replica samplings were subjected to bootstrap analysis (SEQBOOT). The branch lengths are proportional to the evolutionary distance (scale bar) between the taxa. Previously published sequences included and their accession numbers are as follows: HHV6A (X83413); HVS (M31122); HVA3 (AF083424); EBV-B95.8 (V01555); KSHV (U75698); ChRV1 (AJ251573); ChRV2 (AJ251574); RFHVMn (AF005478); RFHVMm (AF005479); RRV/17577 (AF083501); RRV/H26-95 (AF029302); MneRV2 (AF204167); Macaca gamma virus strains from M. mulatta (AF159033), M. fascicularis (AF159032), and M. nemestrina (AF159031), called here MGVMm, MGVMf, and MGVMn, respectively; PanRHV1a (AF250879); PanRHV1b (AF250881); PanRHV2 (AF346490); GorRHV1 (AF250886); MndRHV1 (AF282943); MndRHV2 (AF282937); Cercopithecine hv15 (AY037858); and CalHV-3 (AF319782).