Structure of Chimpanzee Gut Microbiomes across Tropical Africa.

Clifton P Bueno De Mesquita,Christophe Boesch,Emily Neil,Matthew J Gebert,Caihong Vanderburgh,Kyle Yurkiw,Lauren M Nichols,Josephine Head,David Morgan,Els Ton,Badru Mugerwa,Gaëlle Bocksberger,Liliana Pacheco,Volker Sommer,Felix Mulindahabi,Mattia Bessone,Protais Niyigaba,Erin G Wessling,Klaus Zuberbühler,Jack D Lester,Virginie Vergnes,Noah Fierer,Anthony Agbor,Martha M Robbins,Douglas Sheil,Ayuk Emmanuel Ayimisin,Kathryn J Jeffery,Mimi Arandjelovic,Joost Van Schijndel,Lilah Sciaky,Paula Dieguez,Sergio Marrocoli,Maureen S Mccarthy,Roman M Wittig,Aaron Rundus,Paula Álvarez Varona,Bradley Larson,Robert R Dunn,Ammie K Kalan,Juan Lapuente,Villard Ebot Egbe,Heather Cohen,Parag Kadam,Yisa Ginath Yuh,Annemarie Goedmakers,Sorrel Jones,Alex K Piel,Jan F Gogarten,Rebecca Chancellor,Charlotte Coupland,Cyril C Grueter,Hjalmar S Kühl,Tobias Deschner,Crickette Sanz ,R Adriana Hernández‐Aguilar ,M L Kaiser ,Fiona Stewart ,Alexandra N Muellner‐Riehl ,Anne Céline Granjon ,Anna Heintz‐Buschart

doi:10.1128/msystems.01269-20

Abstract

ABSTRACTUnderstanding variation in host-associated microbial communities is important given the relevance of microbiomes to host physiology and health. Using 560 fecal samples collected from wild chimpanzees (Pan troglodytes) across their range, we assessed how geography, genetics, climate, vegetation, and diet relate to gut microbial community structure (prokaryotes, eukaryotic parasites) at multiple spatial scales. We observed a high degree of regional specificity in the microbiome composition, which was associated with host genetics, available plant foods, and potentially with cultural differences in tool use, which affect diet. Genetic differences drove community composition at large scales, while vegetation and potentially tool use drove within-region differences, likely due to their influence on diet. Unlike industrialized human populations in the United States, where regional differences in the gut microbiome are undetectable, chimpanzee gut microbiomes are far more variable across space, suggesting that technological developments have decoupled humans from their local environments, obscuring regional differences that could have been important during human evolution.IMPORTANCE Gut microbial communities are drivers of primate physiology and health, but the factors that influence the gut microbiome in wild primate populations remain largely undetermined. We report data from a continent-wide survey of wild chimpanzee gut microbiota and highlight the effects of genetics, vegetation, and potentially even tool use at different spatial scales on the chimpanzee gut microbiome, including bacteria, archaea, and eukaryotic parasites. Microbial community dissimilarity was strongly correlated with chimpanzee population genetic dissimilarity, and vegetation composition and consumption of algae, honey, nuts, and termites were potentially associated with additional divergence in microbial communities between sampling sites. Our results suggest that host genetics, geography, and climate play a far stronger role in structuring the gut microbiome in chimpanzees than in humans.

Highlights

Explaining differences among individuals and species in microbiome composition, including gut microbiomes, has become a key dimension of research into hostmicrobe interactions and the effects of changes in microbiome on host health and physiology
Humans are an exception to this case, as the important factors of diet and lifestyle can be decoupled from climate and geography, especially in industrialized societies
DNA was extracted from 560 fecal samples collected across the chimpanzee geographic range (Fig. 1), and we used 16S and 18S rRNA marker gene sequence data to characterize the prokaryotic communities and eukaryotic communities, respectively, in each fecal sample

Summary

Introduction

Explaining differences among individuals and species in microbiome composition, including gut microbiomes, has become a key dimension of research into hostmicrobe interactions and the effects of changes in microbiome on host health and physiology. One challenging feature of this work, in humans and other species in which behavior differs among populations, has been to understand the relative importance of dietary choices, environment, geography, and host genetics in structuring microbiomes We consider these factors in light of a species-wide study of the gut microbiomes, including bacteria, archaea, and eukaryotic parasites, of wild chimpanzees (Pan troglodytes) from 29 sites in Africa ranging from 50 km to 5,130 km apart. Similar differences are noted among chimpanzee communities in similar habitats with regard to the consumption of fruits and leaves [35], termites [31], honey [36], algae [30, 37], and some nut species that require tools to crack [29] Such behavioral differences in foraging techniques, presumed to be socially mediated and cultural [38], and consequent differences in diet, may in turn affect gut microbiota composition. The use of tools facilitates access to dietary items that are relatively hard to digest, such as algae (those with stronger cellulose or silica cell walls), and items such as nuts that have unique protein and fat profiles relative to a predominantly fruit- and leaf-based diet

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