Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians

Abstract

Background African 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. Results We 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. Conclusions These 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.

Alteration of the gut fecal microbiome in children living with HIV on antiretroviral therapy in Yaounde, Cameroon

“…In this study we characterize the gut microbiome in a pediatric population of ethnically diverse Cameroonian children with and without HIV. Children living in Cameroon and in SSA broadly have been underrepresented in studies of the gut microbiome, with studies conducted in SSA often focusing on populations with specific lifestyles such as agrarian, pastoralist, or hunter-gathers 4 , 19 – 26 . However, one study conducted in individuals in three populations along an urbanization gradient in Cameroon indicated that urban individuals have retained most of their gut eukaryotic and bacterial diversity despite significant changes in diet compared to the rural areas 27 .…”

“…In Cameroon, customary food staples vary across and within ethnic groups as the preferences for one staple over another are influenced by cultural history/identity and geography 28 . Though some research has investigated the link between subsistence lifestyle and microbiome composition in rural Cameroon 19 , much remains to be discovered about how the interplay between cultural identity, geography, and diet influences microbiome structure and function across Cameroon’s ~ 250 ethnic groups. Unfortunately, during the present study, diet data specific to each community was not collected, and thus constitute a limitation of this study.…”

“…Early investigations in HIV-associated microbiomes reported increases in the Prevotella genus in HIV infected Western populations, but these findings were subsequently shown to be found in high-risk Men who have Sex with Men (MSM) independently of HIV infection status 9 , 10 . The identification of Prevotella strains and their functional differences among different HIV-infected demographics is still an area of active research 19 , 32 – 36 . Since our HIV-infected cohort is on ART, the decrease in Prevotella that we observed here is perhaps consistent with a prior study has found a decrease in Prevotella in HIV-infected individuals with ART 37 .…”

Field evaluation of the gut microbiome composition of pre-school and school-aged children in Tha Song Yang, Thailand, following oral MDA for STH infections

“…But not all STH studies support these findings [22], and their potential pathology has not been determined [16]. One study found that gut microbiome composition was predictive of an STH infection [23]. However, ascribing cause and effect from this finding is not simple, as gut microbial composition may influence susceptibility to STH infection [24].…”

Geographic differences in gut microbiota composition impact susceptibility to enteric infection

“…Fecal microbiota transplants in Italian, US, Canadian, and Dutch populations have proved effective for the treatment of Clostridioides difficile infections (Ianiro et al, 2018;Jiang et al, 2017;Lee et al, 2016;van Nood et al, 2013). Moreover, an individual's gut microbiome composition can predict colonization by gut parasites like Entamoeba and soil-transmitted helminths in rural African populations (Morton et al, 2015;Rubel et al, 2020), and by Vibrio cholera in a pediatric Bangladeshi cohort (Midani et al, 2018). These seminal reports highlight the importance of exploring the causal relationship between the gut microbiome and enteric infections while considering global differences in microbiomes.…”