Assessment of the gorilla gut virome in association with natural simian immunodeficiency virus infection

Mirela D’Arc,Ahidjo Ayouba,Martine Peeters,Juliana D Siqueira,Héctor N Seuánez,Carolina Furtado,Marcelo A Soares

doi:10.1186/s12977-018-0402-9

Abstract

BackgroundSimian immunodeficiency viruses (SIVs) of chimpanzees and gorillas from Central Africa crossed the species barrier at least four times giving rise to human immunodeficiency virus type 1 (HIV-1) groups M, N, O and P. The paradigm of non-pathogenic lentiviral infections has been challenged by observations of naturally infected chimpanzees with SIVcpz associated with a negative impact on their life span and reproduction, CD4+ T-lymphocyte loss and lymphoid tissue destruction. With the advent and dissemination of new generation sequencing technologies, novel promising markers of immune deficiency have been explored in human and nonhuman primate species, showing changes in the microbiome (dysbiosis) that might be associated with pathogenic conditions. The aim of the present study was to identify and compare enteric viromes of SIVgor-infected and uninfected gorillas using noninvasive sampling and ultradeep sequencing, and to assess the association of virome composition with potential SIVgor pathogenesis in their natural hosts.ResultsWe analyzed both RNA and DNA virus libraries of 23 fecal samples from 11 SIVgor-infected (two samples from one animal) and 11 uninfected western lowland gorillas from Campo-Ma’an National Park (CP), in southwestern Cameroon. Three bacteriophage families (Siphoviridae, Myoviridae and Podoviridae) represented 67.5 and 68% of the total annotated reads in SIVgor-infected and uninfected individuals, respectively. Conversely, mammalian viral families, such as Herpesviridae and Reoviridae, previously associated with gut- and several mammalian diseases were significantly more abundant (p < 0.003) in the SIVgor-infected group. In the present study, we analyzed, for the first time, the enteric virome of gorillas and their association with SIVgor status. This also provided the first evidence of association of specific mammalian viral families and SIVgor in a putative dysbiosis context.ConclusionsOur results suggested that viromes might be potentially used as markers of lentiviral disease progression in wild gorilla populations. The diverse mammalian viral families, herein described in SIVgor-infected gorillas, may play a pivotal role in a disease progression still unclear in these animals but already well characterized in pathogenic lentiviral infections in other organisms. Larger sample sets should be further explored to reduce intrinsic sampling variation.

Highlights

Simian immunodeficiency viruses (SIVs) of chimpanzees and gorillas from Central Africa crossed the species barrier at least four times giving rise to human immunodeficiency virus type 1 (HIV-1) groups M, N, O and P
Viral diversity in enteric samples of western lowland gorillas To assess the diversity of the enteric virome of wild gorillas, RNA and DNA libraries of 23 fecal samples from 11 SIVgor-infected and 11 uninfected western lowland gorillas were sequenced
This study suggests that the virome of SIVgor-infected individuals might differ from the one present in uninfected animals, in contrast to what has been reported for the bacteriome in this species [18]

Summary

Introduction

Simian immunodeficiency viruses (SIVs) of chimpanzees and gorillas from Central Africa crossed the species barrier at least four times giving rise to human immunodeficiency virus type 1 (HIV-1) groups M, N, O and P. The human immunodeficiency virus (HIV) types 1 and 2 have arisen from multiple zoonotic transmissions of simian immunodeficiency viruses (SIVs) circulating in African non-human primates (NHP) to humans. SIVs from chimpanzees and gorillas from Central Africa crossed the species barrier at least four times giving rise to HIV-1 groups M, N, O, and P [1, 2]. SIVs have been referred to as immunodeficiency viruses, the clinical manifestations in SIV-infected hosts were not reported during the first decades when natural infections were initially described in the wild and in naturally infected animals, captive sooty mangabeys and African green monkeys kept in zoos or primate centers. Following the experimental or accidental SIV infections of Asian macaques (that are not natural reservoirs of lentiviruses), these latter primates developed an AIDS-like disease that was very similar to the human condition [10, 11]

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