Interactions between parasitic helminths and gut microbiota in wild tropical primates from intact and fragmented habitats

Francesco Rovero,David Modrý,Claudia Barelli,Claudio Donati,Davide Albanese,Barbora Pafčo,Heidi C. Hauffe

doi:10.1038/s41598-021-01145-1

Abstract

The mammalian gastrointestinal tract harbours a highly complex ecosystem composed of a variety of micro- (bacteria, fungi, viruses, protozoans) and macro-organisms (helminths). Although most microbiota research focuses on the variation of single gut components, the crosstalk between components is still poorly characterized, especially in hosts living under natural conditions. We investigated the gut micro-biodiversity (bacteria, fungi and helminths) of 158 individuals of two wild non-human primates, the Udzungwa red colobus (Procolobus gordonorum) and the yellow baboon (Papio cynocephalus). These species have contrasting diets and lifestyles, but live sympatrically in both human-impacted and pristine forests in the Udzungwa Mountains of Tanzania. Using non-invasive faecal pellets, helminths were identified using standard microscopy while bacteria and fungi were characterized by sequencing the V1–V3 variable region of the 16S rRNA gene for bacteria and the ITS1–ITS2 fragment for fungi. Our results show that both diversity and composition of bacteria and fungi are associated with variation in helminth presence. Although interactions differed by habitat type, in both primates we found that Strongyloides was negatively associated and Trichuris was positively associated with bacterial and fungal richness. To our knowledge, this is one of the few studies demonstrating an interaction between helminth and gut microbiota communities in wild non-human primates.

Highlights

The mammalian gastrointestinal tract harbours a highly complex ecosystem composed of a variety of micro- and macro-organisms
A few recent studies have evaluated the diversity and composition of the gut bacterial communities of non-human primates naturally infected by h elminths[36,37,38,39], here we compare both the bacterial and fungal components in helminth-positive and helminth-negative individuals to investigate: (i) whether bacterial and fungal richness and/or composition vary in primates with different ecological adaptations residing in either pristine or human-impacted forests; (ii) which bacterial and fungal taxa are responsible for such variation; and (iii) which of the detected helminths interplay with bacterial and fungal richness
This paper investigated the interactions between helminth presence and gut microbiota components in two primate species living in two forest types

Summary

Introduction

The mammalian gastrointestinal tract harbours a highly complex ecosystem composed of a variety of micro- (bacteria, fungi, viruses, protozoans) and macro-organisms (helminths). Of the hosts (e.g. dampening allergic responses and ameliorating of gut dysfunction in humans29), investigating the gut communities of animal species closely related to humans (i.e. non-human primates) living under natural conditions is of particular relevance Studies of these associations will provide a critical foundation to understanding the potential mechanisms that underpin the interplay between helminths, microbiota and hosts, and will deepen our awareness of animal health with possible conservation implications. A few recent studies have evaluated the diversity and composition of the gut bacterial communities of non-human primates naturally infected by h elminths[36,37,38,39], here we compare both the bacterial and fungal components in helminth-positive and helminth-negative individuals to investigate: (i) whether bacterial and fungal richness and/or composition vary in primates with different ecological adaptations residing in either pristine or human-impacted forests; (ii) which bacterial and fungal taxa are responsible for such variation; and (iii) which of the detected helminths interplay with bacterial and fungal richness

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Results

Discussion

Conclusion