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

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.

Detangling the Crosstalk Between Ascaris, Trichuris and Gut Microbiota: What´s Next?

“…Many of the results found in previously described animal models have been consistent with those evidenced in studies with human populations. Lee et al., 2014 , conducted an analysis in an indigenous human population in Malaysia, where they observed an increase in the diversity and abundance of the intestinal microbiota in Trichuris -infected subjects, with a preponderance of members of the Paraprevotellaceae family, raising evidence that helminths may have an impact in modulating diversity, bacterial community structure and function of the intestinal microbiota of human hosts, being consistent with findings in mice and primates ( Lee et al., 2014 ; Houlden et al., 2015 ; Barelli et al., 2021 ). Interestingly, a previous study carried by Lee et al.…”

“…was associated with a higher bacterial richness and diversity. These findings could have a relevant ecological impact on different primate populations, highlighting again the importance of interactions between helminths and host microbiota ( Barelli et al., 2021 ).…”

A comparison of rectal and oral cultivable microbiota in wild and captive black lion tamarins (Leontopithecus chrysopygus, Mikan 1823)

“…More information is needed to understand the microbial composition of healthy gut microbiota in wild and captive nonhuman primates. For example, studies of antimicrobial resistance and social environment are crucial to connect microbiotal information to animal health (Barelli et al, 2021; Bornbusch & Drea, 2021; García et al, 2020; Kuthyar et al, 2019; Perofsky et al, 2017; Sarkar et al, 2020; Tsukayama et al, 2018; Tung et al, 2015; Zhu et al, 2021; Zvoboda, 2017). A decrease in the diversity of intestinal microbiome species may be associated with diseases and inflammation thus aiding pathogenic microorganisms (Battaglioli et al, 2018; Cho & Blaser, 2012; Hale et al, 2019; Petersen & Round, 2014).…”

Investigation of Host–Microbe–Parasite Interactions in an In Vitro 3D Model of the Vertebrate Gut

“…Interestingly, recent findings associate infections by gastrointestinal helminths with higher gut microbiota species richness and diversity, which in turn is associated with a “healthier” intestinal homeostasis. [ 90 ] Although it is well accepted that worms contribute to the development and regulation of the immune system via multifactorial mechanisms, these are not yet fully understood. One hypothesis, corroborated by data from several studies in humans and animal models of worm infection, is that host–microbiome–parasite interactions are modulated directly or indirectly by helminth ESP, a mixture of bioactive components secreted by the parasite that span proteins, lipids, carbohydrates, nucleic acids, and metabolites, essential for helminth life cycle (e.g., feeding, host invasion).…”