The microbiome of the human facial skin is unique compared to that of other hominids

Abstract

The human facial skin microbiome is remarkably similar across all people sampled to date, dominated by facultative anaerobe Cutibacterium. The origin of this genus is unknown, with no close relatives currently described from samples of primate skin. This apparent human-specific bacterial taxon could reflect the unique nature of human skin, which is significantly more oily than that of our closest primate relatives. However, previous studies have not sampled the facial skin microbiome of our closest primates. Here, we profiled the skin microbiome of zoo-housed chimpanzees (Pan troglodytes), and gorillas (Gorilla gorilla gorilla), alongside their human care staff, using both 16S and shotgun sequencing. We showed that facial skin microbiomes differ significantly across host species, with humans having the lowest diversity and most unique community among the three species. We were unable to find a close relative of Cutibacterium on either chimpanzee or gorilla facial skin, consistent with human-specificity. Hominid skin microbiome functional profiles were more functionally similar compared to their taxonomic profiles. However, we still found notable functional differences including lower proportions of fatty acid biosynthesis on humans, consistent with microbes reliance on host-derived lipids. Our study highlights the uniqueness of the human facial skin microbiome and supports a horizontal acquisition of its dominant resident from a yet unknown source. ImportanceUnderstanding how and why human skin bacteria differ from our closest animal relatives provides crucial insights into human evolution and health. While we have known that human facial skin hosts distinct bacteria--particularly Cutibacterium acnes--we did not know if these bacteria and their associated genes were also present on the faces of our closest relatives, chimpanzees and gorillas. Our study shows that human facial skin hosts markedly different bacteria than other primates, with C. acnes being uniquely abundant on human faces. This finding suggests that this key bacterial species may have adapted specifically to human skin, which produces more oils than other primates.