Assessing the Influence of Environmental Sources on the Gut Mycobiome of Tibetan Macaques

Abstract

The distribution and availability of microbes in the environment has an important effect on the composition of the gut microbiome of wild vertebrates. However, our current knowledge of gut-environmental interactions is based principally on data from the host bacterial microbiome, rather than on links that establish how and where hosts acquire their gut mycobiome. This complex interaction needs to be clarified. Here, we explored the relationship between the gut fungal communities of Tibetan macaques (Macaca thibetana) and the presence of environmental (plant and soil) fungi at two study sites using the fungal internal transcribed spacer (ITS) and next generation sequencing. Our findings demonstrate that the gut, plant and soil fungal communities in their natural habitat were distinct. We found that at both study sites, the core abundant taxa and ASVs (Amplicon Sequence Variants) of Tibetan macaques’ gut mycobiome were present in environmental samples (plant, soil or both). However, the majority of these fungi were characterized by a relatively low abundance in the environment. This pattern implies that the ecology of the gut may select for diverse but rare environmental fungi. Moreover, our data indicates that the gut mycobiome of Tibetan macaques was more similar to the mycobiome of their plant diet than that present in the soil. For example, we found three abundant ASVs (Didymella rosea, Cercospora, and Cladosporium) that were present in the gut and on plants, but not in the soil. Our results highlight a relationship between the gut mycobiome of wild primates and environmental fungi, with plants diets possibly contributing more to seeding the macaque’s gut mycobiome than soil fungi.

The primate gut mycobiome-bacteriome interface is impacted by environmental and subsistence factors

“…This contention is further supported by our findings: weaker influence of phylogenetic constraints and higher inter-individual variability within groups in mycobiome composition, weak correspondence between fungal and bacterial community assemblies, and inconsistent nature of interactions observed between fungi and bacteria in the primate gut. In line with these data, the strong influence of dietary and environmental sources in seeding the gut mycobiome has been reported recently in mice 10 and nonhuman primates 16,25,26 . Compared with the bacteriome, the gut environment may be particularly susceptible to food-derived and environmental fungi, albeit transiently 27 , possibly triggering the heterogeneous compositional patterns we observed between individuals within the same primate population.…”

“…Instead, wild lowland gorillas shared mycobiome similarity with wild chimpanzees and wild agile mangabeys, which are more phylogenetically divergent. Mycobiome convergence between these wild primate populations could be explained by similar feeding behaviors, specifically by a similar degree of reliance on fruit [31][32][33] , but also by environmental seeding sources from plants and soil shared in a common niche 16,25 . However, selectivity and preference of specific fruit substrates vary greatly among wild primates, even when sharing the same location and resources, which may explain whyalthough a mycobiome overlap was observed between these three species -each shows a set of unique indicator fungal taxa.…”

Effects of captive and primate-focused tourism on the gut microbiome of Tibetan macaques

“…For the tourism group of Tibetan macaque used in this study, a small amount of corn provided by staff each day, but feeding from tourists were forbidden strictly. Although the group has been a subject of over 30 years for behavioral research and primate-focused tourism ( Li and Kappeler, 2020 ), individuals of this group still maintain a direct interface with natural environment, and getting their food and water from sources which contain complexity of microbial communities ( Sun et al, 2021b ). Our result demonstrated that living in the wild and consuming natural diet could maintain the gut bacterial diversity of tourism group, which is consistent with our previous study on gut mycobiome in Tibetan macaques ( Sun et al, 2021a ).…”

Maternal and infantile gut mycobiome during the weaning period in free ranging Tibetan macaques (Macaca thibetana)

“…Environmental fungi are one of the main sources of gut mycobiome in mammals, especially the fungi carried by food resources. Our previous study has showed that the plant pathogen was dominant fungal guilds of gut mycobiome in Tibetan macaques (Sun, Xia, Davison, et al, 2021; Sun, Xia, Garber, et al, 2021), and plants diets possibly contributing more to seeding the macaque's gut mycobiome than soil fungi (Sun, Xia, Davison, et al, 2021; Sun, Xia, Garber, et al, 2021). We speculate that the increased in plant pathogens in the post‐weaning period of infant Tibetan macaques should be due to their completely plant diet like the adult individuals.…”