The ocular surface microbiome of rhesus macaques

The ocular surface microbiota (OSM) is important for eye health, and variations in OSM composition have been associated with multiple diseases in humans. Studies of OSM-disease dynamics in humans are confounded by lifestyle factors. Animal models provide a complementary approach to understanding biological systems, free from many confounds of human studies. Here, we provide the first study of the OSM of rhesus macaques, a premier animal model for eye health and disease. We describe the taxonomy of the rhesus macaque OSM, and explore compositional correlations with age, sex, and living condition.

We analyzed eyelid and conjunctival microbiota swabs from 132 individual rhesus macaques (Macaca mulatta) (57 males, 75 females, 1-26 years old) from one captive and one free-ranging group using 16 S rRNA V3/V4 MiSeq sequencing. We investigated alpha diversity, beta diversity, and differential abundance.

We found several similarities between the top Phyla and Genera of the rhesus macaque OSM and those reported in human literature. Significantly higher alpha diversity, which may reflect age-related ocular surface mucous membrane integrity and immune function, was present in younger individuals compared to older ones. Higher alpha diversity was also present in free-ranging rhesus macaques compared to ones in captivity, possibly related to differences in diet, exercise, and medical exposures between macaques in different living conditions. Beta diversity was most strongly influenced by individual identity, followed by living conditions. Sex did not correlate with any OSM variation.

In this study we describe the taxonomic composition of the rhesus macaque OSM, and identify significant differences in alpha and beta diversity according to individual nonhuman primate host variables and the surrounding environment. Our findings suggest composition of the nonhuman primate OSM is shaped by age-related physiology, individual identity, and external living conditions. Our results offer novel insights into an underexplored region of the primate microbiome and highlight the utility of rhesus macaques as a model system for investigating the links between the OSM, ocular health, and disease.