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

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

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 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. We 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. Our 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.