Biodiversity of protists and nematodes in the wild nonhuman primate gut

Allison E Mann,Rebecca J Lewis,Andrea L Baden,Andrés Link,Evan Morien,Stacey R Tecot ,Matthew A Lemay,Frank P Cuozzo,Anthony Di Fiore,Rebecca M Stumpf ,Larissa Swedell,Vincent Billy,Nathaniel J Dominy,Martín M Kowalewski ,Michelle L Sauther,Andrés Gómez ,Florent Mazel,Gillian A.o Rice ,Tony L Goldberg,Katherine R Amato ,Laura Wegener Parfrey

doi:10.1038/s41396-019-0551-4

Abstract

Documenting the natural diversity of eukaryotic organisms in the nonhuman primate (NHP) gut is important for understanding the evolution of the mammalian gut microbiome, its role in digestion, health and disease, and the consequences of anthropogenic change on primate biology and conservation. Despite the ecological significance of gut-associated eukaryotes, little is known about the factors that influence their assembly and diversity in mammals. In this study, we used an 18S rRNA gene fragment metabarcoding approach to assess the eukaryotic assemblage of 62 individuals representing 16 NHP species. We find that cercopithecoids, and especially the cercopithecines, have substantially higher alpha diversity than other NHP groups. Gut-associated protists and nematodes are widespread among NHPs, consistent with their ancient association with NHP hosts. However, we do not find a consistent signal of phylosymbiosis or host-species specificity. Rather, gut eukaryotes are only weakly structured by primate phylogeny with minimal signal from diet, in contrast to previous reports of NHP gut bacteria. The results of this study indicate that gut-associated eukaryotes offer different information than gut-associated bacteria and add to our understanding of the structure of the gut microbiome.

Highlights

Comparative studies of gut microbiome structure across phylogenetically similar but ecologically distinct host species help clarify factors that regulate microbial community assembly, structure, and stability over time
Eukaryotic taxa detected across nonhuman primate (NHP) species include organisms that reside in the gut along with many non-gut residents
While we aim to study only true NHP gut residents, identifying them is dependent on the taxonomic resolution of the data as well as a priori knowledge of which organisms colonize the NHP gut

Summary

Introduction

Comparative studies of gut microbiome structure across phylogenetically similar but ecologically distinct host species help clarify factors that regulate microbial community assembly, structure, and stability over time. In mammals, these patterns are shaped by a variety of factors including host gut physiology, diet, phylogeny [1,2,3,4,5,6], host age, geography [7, 8], and social behavior [9, 10]. Because C. albicans reportedly colonizes the gut of healthy humans [24,25,26], antagonistic relationships between eukaryotes and other microbes may promote gut homeostasis

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