Arteriviruses, Pegiviruses, and Lentiviruses Are Common among Wild African Monkeys

Abstract

Nonhuman primates (NHPs) are a historically important source of zoonotic viruses and are a gold-standard model for research on many human pathogens. However, with the exception of simian immunodeficiency virus (SIV) (family Retroviridae), the blood-borne viruses harbored by these animals in the wild remain incompletely characterized. Here, we report the discovery and characterization of two novel simian pegiviruses (family Flaviviridae) and two novel simian arteriviruses (family Arteriviridae) in wild African green monkeys from Zambia (malbroucks [Chlorocebus cynosuros]) and South Africa (vervet monkeys [Chlorocebus pygerythrus]). We examine several aspects of infection, including viral load, genetic diversity, evolution, and geographic distribution, as well as host factors such as age, sex, and plasma cytokines. In combination with previous efforts to characterize blood-borne RNA viruses in wild primates across sub-Saharan Africa, these discoveries demonstrate that in addition to SIV, simian pegiviruses and simian arteriviruses are widespread and prevalent among many African cercopithecoid (i.e., Old World) monkeys. IMPORTANCEPrimates are an important source of viruses that infect humans and serve as an important laboratory model of human virus infection. Here, we discover two new viruses in African green monkeys from Zambia and South Africa. In combination with previous virus discovery efforts, this finding suggests that these virus types are widespread among African monkeys. Our analysis suggests that one of these virus types, the simian arteriviruses, may have the potential to jump between different primate species and cause disease. In contrast, the other virus type, the pegiviruses, are thought to reduce the disease caused by human immunodeficiency virus (HIV) in humans. However, we did not observe a similar protective effect in SIV-infected African monkeys coinfected with pegiviruses, possibly because SIV causes little to no disease in these hosts.

Semi‐quantitative duplex RT ‐ PCR reveals the low occurrence of Porcine Pegivirus and Atypical Porcine Pestivirus in diagnostic samples from the United States

“…Pegiviruses are divided into 11 species ( Pegivirus A‐K ) (Smith et al., ) and have been identified from a variety of mammalian species including human, baboons, chimpanzees, monkeys, tamarins, bats, camels, horses, rodents and pigs (Tang et al., ; Thézé, Lowes, Parker, & Pybus, ). Pegiviruses have been detected in North and South America, Africa, Asia and Europe, indicating global presence of this virus (Bailey et al., ; de Souza et al., ; N'Guessan et al., ; Thézé et al., ; Van Nguyen et al., ). In 2016, Porcine Pegiviruses (PPgV) were discovered in pigs from Germany using Next Generation Sequencing (NGS) of serum from asymptomatic animals, and subsequent PCR testing detected PPgV in 2.2% of serum samples (Baechlein et al., ).…”

Within-Host Evolution of Simian Arteriviruses in Crab-Eating Macaques

“…KRCV-1 has not been detected in any other primate species of African or Asian origin besides red colobus monkeys, either in captivity or in the wild, despite screens of captive macaques and wild nonhuman primates from Kibale National Park. However, additional highly divergent simian arteriviruses have recently been discovered in apparently healthy wild red-tailed monkeys (Cercopithecus ascanius) (12), yellow baboons (Papio cynocephalus) (13), hybrid kinda ϫ grayfooted-chacma baboons (Papio kindae ϫ Papio ursinus griseipes) (14), malbroucks (Chlorocebus cynosuros), African green monkeys (Chlorocebus aethiops) (15), vervet monkeys (Chlorocebus pygerythrus) (15), and De Brazza's monkeys (Cercopithecus neglectus) (10), indicating that these viruses are widespread among African monkeys. We recently analyzed samples collected during three separate SHF outbreaks that occurred in captive macaque colonies in the 1960s and late 1980s.…”

Genome-wide patterns of gene expression in a wild primate indicate species-specific mechanisms associated with tolerance to natural simian immunodeficiency virus infection

“…Viral load (reported as log 10 genome copies per mL of plasma) estimates were similar between the env and LTR RT-qPCR assays (Mann Whitney U = 94, Z = -1.24, p = 0.22; Figure 1). There were no significant differences between males and females for either env (t(10)= 1.06, p = 0.31) or LTR (t(10) = 0.66, p = 0.26), and viral load for both measures were within the range of those reported using RT-qPCR of the viral int protein for three species of naturally SIV-infected AGMs (Bailey et al 2016a;Ma et al, 2014; Figure 1).…”

“…Natural populations of Ugandan red colobus (URC; Piliocolobus tephrosceles; Old World monkey subfamily Colobinae) have emerged as an important wild primate species for understanding the role of host biology in viral disease (Bailey et al, , 2016a(Bailey et al, , 2016bGoldberg et al, 2008Goldberg et al, , 2009Ladner et al, 2016;Lauck et al, 2011Lauck et al, , 2013Sibley et al, 2014). SIV diversity in red colobus was first described in western red colobus (Piliocolobus badius) in Taï forest in Côte d' Ivoire and established the red colobus as a potential reservoir for viral transmission to humans (Locatelli et al, 2008a).…”