Intestivirid Acquisition Increases Across Infancy in a Wild Primate Population

Abstract

Intestivirids (order Crassvirales, family Intestiviridae), viruses that infect Bacteroidales bacteria in the mammalian gastrointestinal tract, have been identified as a highly abundant component of the healthy human virome that may shape patterns of human health and disease through direct action on the microbiome. While double-stranded DNA bacteriophages called crAssphages (Carjivirus communis) that infect bacteria in the Bacteroidales order have been identified in humans within the first month of life, the enormous variation in post-parturition infant environments and diets has inhibited a robust understanding of the physiological and environmental factors that govern acquisition patterns. We turned to a wild population of graminivorous nonhuman primates (geladas, Theropithecus gelada) under long-term study in the Simien Mountains National Park, Ethiopia, analysing faecal samples from infants and mothers in this population across the infancy period for richness and presence of crAssphage-like viruses (family Intestiviridae). Eight intestivirid genomes were identified based on terminal redundancy representing six unique variants (< 98% intergenomic similarity) closely related to the human crAssphage. The prevalence of intestivirids in gelada faecal samples begins to rise at about 10 months of age, peaks in the months surrounding weaning (~18 months), and somewhat decreases but maintains high levels into adulthood. We found a strong association between cumulative rainfall and intestivirid detection, with a higher likelihood accompanying wetter seasons with higher grass availability. In this population, the months prior to weaning have been found to be accompanied by a shift in the microbiome characterised by a decrease in glycan degrader Bacteroidales taxa and an increase in fermentative Bacteroidales taxa, and wetter seasons when the vast majority of the gelada diet comprises grasses are associated with an increase in fermentative Bacteroidales taxa. In the context of these microbiome shifts, our results suggest that the intestivirid-bacterial host relationship may interact with major developmental and seasonal dietary shifts in the mammalian host.

Keywords: Theropithecus gelada; Crassvirales; Intestiviridae; bacteriophage; primate virome; geladas.