Abstract
BackgroundAfrican populations provide a unique opportunity to interrogate host-microbe co-evolution and its impact on adaptive phenotypes due to their genomic, phenotypic, and cultural diversity. We integrate gut microbiome 16S rRNA amplicon and shotgun metagenomic sequence data with quantification of pathogen burden and measures of immune parameters for 575 ethnically diverse Africans from Cameroon. Subjects followed pastoralist, agropastoralist, and hunter-gatherer lifestyles and were compared to an urban US population from Philadelphia.ResultsWe observe significant differences in gut microbiome composition across populations that correlate with subsistence strategy and country. After these, the variable most strongly associated with gut microbiome structure in Cameroonians is the presence of gut parasites. Hunter-gatherers have high frequencies of parasites relative to agropastoralists and pastoralists. Ascaris lumbricoides, Necator americanus, Trichuris trichiura, and Strongyloides stercoralis soil-transmitted helminths (“ANTS” parasites) significantly co-occur, and increased frequency of gut parasites correlates with increased gut microbial diversity. Gut microbiome composition predicts ANTS positivity with 80% accuracy. Colonization with ANTS, in turn, is associated with elevated levels of TH1, TH2, and proinflammatory cytokines, indicating an association with multiple immune mechanisms. The unprecedented size of this dataset allowed interrogation of additional questions—for example, we find that Fulani pastoralists, who consume high levels of milk, possess an enrichment of gut bacteria that catabolize galactose, an end product of lactose metabolism, and of bacteria that metabolize lipids.ConclusionsThese data document associations of bacterial microbiota and eukaryotic parasites with each other and with host immune responses; each of these is further correlated with subsistence practices.
Highlights
African populations provide a unique opportunity to interrogate hostmicrobe co-evolution and its impact on adaptive phenotypes due to their genomic, phenotypic, and cultural diversity
We compare the associations of parasite burden with the gut microbiome structure, first using 16S rRNA gene tag sequencing and using shotgun metagenomics
As subsistence and ethnicity are strongly correlated in these populations, only subsistence was included as a statistical parameter in the analyses described below
Summary
African populations provide a unique opportunity to interrogate hostmicrobe co-evolution and its impact on adaptive phenotypes due to their genomic, phenotypic, and cultural diversity. We integrate gut microbiome 16S rRNA amplicon and shotgun metagenomic sequence data with quantification of pathogen burden and measures of immune parameters for 575 ethnically diverse Africans from Cameroon. There is a need to characterize the consequences of gastrointestinal parasite colonization and infection [1] in rural populations living traditional lifestyles to understand their effects on health [2]. We focus on populations from Cameroon that are genetically, linguistically, phenotypically, and culturally diverse [16,17,18,19,20]. These populations have different types of subsistence practices but share overlapping environments and high infectious disease burdens. We present a detailed analysis of sequence data from gut microbiota, quantitative measurements of multiple pathogen loads, host immune parameters, and extensive demographic data for 575 Cameroonian subjects
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