Identification and characterization of highly divergent simian foamy viruses in a wide range of new world primates from Brazil.

Cláudia P Muniz,William M Switzer,Hongwei Jia,Alcides Pissinatti,Héctor N Seuánez,Bechan Sharma,Cibele R Bonvicino,Marcelo A Soares,Miguel A Moreira,Lian L Troncoso,Anupama Shankar,André F Santos,Esmeralda A Soares

doi:10.1371/journal.pone.0067568

Abstract

Foamy viruses naturally infect a wide range of mammals, including Old World (OWP) and New World primates (NWP), which are collectively called simian foamy viruses (SFV). While NWP species in Central and South America are highly diverse, only SFV from captive marmoset, spider monkey, and squirrel monkey have been genetically characterized and the molecular epidemiology of SFV infection in NWPs remains unknown. We tested a large collection of genomic DNA (n = 332) comprising 14 genera of NWP species for the presence of SFV polymerase (pol) sequences using generic PCR primers. Further molecular characterization of positive samples was carried out by LTR-gag and larger pol sequence analysis. We identified novel SFVs infecting nine NWP genera. Prevalence rates varied between 14–30% in different species for which at least 10 specimens were tested. High SFV genetic diversity among NWP up to 50% in LTR-gag and 40% in pol was revealed by intragenus and intrafamilial comparisons. Two different SFV strains infecting two captive yellow-breasted capuchins did not group in species-specific lineages but rather clustered with SFVs from marmoset and spider monkeys, indicating independent cross-species transmission events. We describe the first SFV epidemiology study of NWP, and the first evidence of SFV infection in wild NWPs. We also document a wide distribution of distinct SFVs in 14 NWP genera, including two novel co-speciating SFVs in capuchins and howler monkeys, suggestive of an ancient evolutionary history in NWPs for at least 28 million years. A high SFV genetic diversity was seen among NWP, yet these viruses seem able to jump between NWP species and even genera. Our results raise concerns for the risk of zoonotic transmission of NWP SFV to humans as these primates are regularly hunted for food or kept as pets in forest regions of South America.

Highlights

Foamy viruses (FV) are complex retroviruses in the Spumavirus genus that naturally infect a wide range of mammals, including bovines, felines, equines, sheep, and nonhuman primates (NHPs)
The assay was validated using peripheral blood lymphocyte DNA from 47 seronegative and 59 seropositive New World primates (NWP) identified using a Western blot (WB) test that utilizes simian foamy viruses (SFV) antigens from marmoset and spider monkeys grown in Cf2Th cells
The 105 NWPs used for the PCR assay validation were all housed at various US institutions. Genomic DNA (gDNA) was available from seven genera of NWPs including Cebus, Alouatta, Callithrix, Aotus, Ateles, Saimiri, Cacajao and Pithecia

Summary

Introduction

Foamy viruses (FV) are complex retroviruses in the Spumavirus genus that naturally infect a wide range of mammals, including bovines, felines, equines, sheep, and nonhuman primates (NHPs). In NHPs, FV are referred to as simian foamy viruses (SFV) Their unusual name refers to the formation of syncytia of multinucleated giant cells with numerous vacuoles seen by electron microscopy with a foamy appearance upon virus infection in vitro [1]. While SFV isolates have been identified in numerous, diverse species of African and Asian NHPs [3,4,5,6,7], or Catarrhini, humans do not appear to be a natural host of these viruses. All SFVs detected in humans were acquired by zoonotic transmission from infected African and Asian NHPs and far are persistent but seemingly asymptomatic infections [2,8,9,10,11,12]. Persons infected with SFV while working with NHPs in biomedical facilities have been reported with prevalence ranging from 3–4% [9,14,15]

Methods

Results

Conclusion