Variation in rural African gut microbiomes is strongly shaped by parasitism and diet

Abstract

The human gut microbiome is influenced by its host’s nutrition and health status, and represents an interesting adaptive phenotype under the influence of metabolic and immune constraints. Previous studies contrasting rural populations in developing countries to urban industrialized ones have shown that geography is an important factor associated with the gut microbiome; however, studies have yet to disentangle the effects of factors such as climate, diet, host genetics, hygiene and parasitism. Here, we focus on fine-scale comparisons of African rural populations in order to (i) contrast the gut microbiomes of populations that inhabit similar environments but have different traditional subsistence modes and (ii) evaluate the effect of parasitism on microbiome composition and structure. We sampled rural Pygmy hunter-gatherers as well as Bantu individuals from both farming and fishing populations in Southwest Cameroon and found that the presence of Entamoeba is strongly correlated with microbial composition and diversity. Using a random forest classifier model, we showed that an individual’s infection status can be predicted with 79% accuracy based on his/her gut microbiome composition. We identified multiple taxa that differ significantly in frequency between infected and uninfected individuals, and found that alpha diversity is significantly higher in infected individuals, while beta-diversity is reduced. Another factor associated with microbial composition in our data is subsistence mode, notably with some taxa previously shown to differ between Hadza Eastern African hunter-gatherers and Italians also discriminating Pygmy hunter-gatherers from Cameroon from neighboring farming or fishing populations. In conclusion, our results stress the importance of taking into account an individual’s parasitism status in studies of the microbiome, and highlight how sensitive the microbial ecosystem is to subtle changes in host nutrition. Our fine-scale analysis allowed us to identify microbial features that are specific to hunter-gatherers versus ones shared by all rural African populations, increasing our understanding of the influence of subsistence mode and lifestyle on gut microbiome composition.