Ecological and evolutionary adaptations shape the gut microbiome of BaAka African rainforest hunter-gatherers

Gómez, Andrés; Petrželková, Klára J.; Yeoman, CJ; Mb, Burns; Kr, Amato; Vlčková, Klára; Modrý, David; Todd, Angelique; Ca, Jost Robbinson; Remis, Melissa J.; Torralba, Manolito; Ke, Nelson; Carbonero, Franck; Hr, Gaskins; Ba, Wilson; Rm, Stumpf; Ba, White; Leigh,; Blekhman, Ran

doi:10.1101/019232

“…The hunter-gatherers were correctly assigned to their subsistence mode with higher accuracy (85%) relative to the other populations. Furthermore, some of our findings mirror patterns previously observed in comparisons of traditional vs. industrialized societies [ 18 , 20 , 26 , 48 ] (see Table 1 ), suggesting this ancestral subsistence mode might carry a specific microbial signature. Notably, we found a higher frequency of Proteobacteria in hunter-gatherers compared to the other Cameroonian populations, similar to the relationship between the Hadza and Italians [ 18 ] and that between traditional populations in Peru (hunter-gathers and farmers) and US individuals [ 20 ].…”

Section: Discussionsupporting

confidence: 87%

“…Furthermore, Ruminococcaceae uncl was shown to be enriched in Hadza as compared to Italians [ 18 ]. Spirochaetaceae Treponema , the third most important taxon, include species that have been reported to inhabit the cow rumen, the pig gastrointestinal tract, and the guts of termites [ 47 ] and have been proposed as symbionts in the human “ancestral microbiome” [ 18 , 20 , 48 ]. Christensenellaceae , the fourth most important taxon, was recently identified as being the most heritable taxon in an analysis of twins from the UK, and was shown to impact host metabolism [ 5 ].…”

Section: Resultsmentioning

confidence: 99%

Variation in Rural African Gut Microbiota Is Strongly Correlated with Colonization by Entamoeba and Subsistence

Morton

¹

,

Lynch

²

,

Froment

³

et al. 2015

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The human gut microbiota is impacted by host nutrition and health status and therefore represents a potentially adaptive phenotype influenced by metabolic and immune constraints. Previous studies contrasting rural populations in developing countries to urban industrialized ones have shown that industrialization is strongly correlated with patterns in human gut microbiota; however, we know little about the relative contribution of factors such as climate, diet, medicine, hygiene practices, host genetics, and parasitism. Here, we focus on fine-scale comparisons of African rural populations in order to (i) contrast the gut microbiota of populations inhabiting similar environments but having different traditional subsistence modes and either shared or distinct genetic ancestry, and (ii) examine the relationship between gut parasites and bacterial communities. Characterizing the fecal microbiota of Pygmy hunter-gatherers as well as Bantu individuals from both farming and fishing populations in Southwest Cameroon, we found that the gut parasite Entamoeba is significantly correlated with microbiome composition and diversity. We show that across populations, colonization by this protozoa can be predicted with 79% accuracy based on the composition of an individual's gut microbiota, and that several of the taxa most important for distinguishing Entamoeba absence or presence are signature taxa for autoimmune disorders. We also found gut communities to vary significantly with subsistence mode, notably with some taxa previously shown to be enriched in other hunter-gatherers groups (in Tanzania and Peru) also discriminating hunter-gatherers from neighboring farming or fishing populations in Cameroon.

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“…The hunter-gatherers were correctly assigned to their subsistence mode with higher accuracy (85%) relative to the other populations. Furthermore, some of our findings mirror patterns previously observed in comparisons of traditional vs. industrialized societies (18,20,26,48) (see Table 1b), suggesting this ancestral subsistence mode might carry a specific microbial signature. Notably, we found a higher frequency of Proteobacteria in hunter-gatherers compared to the other Cameroonian populations, similar to the relationship between the Hadza and Italians (18) and that between traditional populations in Peru (hunter-gathers and farmers) and US individuals (20).…”

Section: Influence Of Subsistence and Genetic Ancestrysupporting

confidence: 86%

“…Spirochaetaceae Treponema, the third most important taxon, include species that have been reported to inhabit the cow rumen, the pig gastrointestinal tract, and the guts of termites (47) and have been proposed as symbionts in the human "ancestral microbiome" (18,20,48).…”

Section: Relationship Between Parasitism and The Microbiomementioning

confidence: 99%

Variation in rural African gut microbiota is strongly correlated with colonization byEntamoebaand subsistence

Morton

¹

,

Lynch

²

,

Froment

³

et al. 2015

Preprint

Self Cite

View full text Add to dashboard Cite

The human gut microbiota is impacted by host nutrition and health status and therefore represents a potentially adaptive phenotype influenced by metabolic and immune constraints. Previous studies contrasting rural populations in developing countries to urban industrialized ones have shown that industrialization is strongly correlated with patterns in human gut microbiota; however, we know little about the relative contribution of factors such as climate, diet, medicine, hygiene practices, host genetics, and parasitism. Here, we focus on finescale comparisons of African rural populations in order to (i) contrast the gut microbiota of populations inhabiting similar environments but having different traditional subsistence modes and either shared or distinct genetic ancestry, and (ii) examine the relationship between gut parasites and bacterial communities. Characterizing the fecal microbiota of Pygmy hunter-gatherers as well as Bantu individuals from both farming and fishing populations in Southwest Cameroon, we found that the gut parasite Entamoeba is significantly correlated with microbiome composition and diversity. We show that across populations, colonization by this protozoa can be predicted with 79% accuracy based on the composition of an individual's gut microbiota, and that several of the taxa most important for distinguishing Entamoeba absence or presence are signature taxa for autoimmune disorders. We also found gut communities to vary significantly with subsistence mode, notably with some taxa previously shown to be enriched in other hunter-gatherers groups (in Tanzania and Peru) also discriminating hunter-gatherers from neighboring farming or fishing populations in Cameroon. Funding: This work was funded by the Howard Hughes Medical Institute (HHMI) and the French National Agency for Research (ANR; grant ANR-11-BSV7-0011). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Competing Interests: The authors declared that no competing interests exist. Author SummaryThe community of microorganisms inhabiting the gastrointestinal tract plays a critical role in determining human health. It's been hypothesized that the industrialized lifestyle, marked by a diet rich in processed foods, higher use of antibiotics, increased hygiene, and exposure to various chemicals, has altered microbiota in ways that are harmful. Studies have addressed this by comparing rural and industrialized populations, and have found that they systematically vary in their gut microbiome composition. Nevertheless, the relative influence of host genetics, diet, climate, medication, hygiene practices, and parasitism is still not clear. In addition, microbial variation between nearby human populations has not been explored in depth. Moreover, The World Health Organization estimates that 24% of the world's population, concentrated in developing countries, is infected with gut parasites. Despite this, and evidence for direct interactions between the immune syste...

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“…Lifestyle has a major impact on the composition of the gut microbiome [1,2]. It has been showed that urban populations have a different composition of the gut microbiome than that of rural populations [3][4][5][6].…”

Section: Introductionmentioning

confidence: 99%

Prevalence of Treponema species in the Gut Microbiome is Linked to Bifidobacterium sp. and Bacteroides sp.

Belkacemi¹,

Alou²,

Million³

et al. 2020

Preprint

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BackgroundTreponema species as commensals of the human microbiome have a prevalence and function depending on the studied niche. In the oral cavity, treponemes are ubiquitous while they have been strictly linked to rural and ancestral populations in the gastro-intestinal tract and are undetected in urban populations. In this study, an in silico analysis of 1481 metagenomes, selected based on the previous detection of treponemes in such sample types, was conducted to predict putative bacterial antagonists of treponemes, i.e. bacteria present when treponemes are lacking and vice versa. Predicted antagonists were subsequently tested in-vitro against Treponema denticola CSUR P7640.ResultsMost frequent predicted antagonists included members of the Bifidobacteriaceae family (23.3%) among which Bifidobacterium longum was the most significant (63.3% in T- group, p <0.0000001) as well as members of the Bacteroides (6.7%) and Streptococcus (13.3%) genera. The relative abundance of the aforementioned taxa was also anticorrelated with that of the Treponema genus in the metagenomes analyzed in this study. B. longum CSUR P7400, Bifidobacterium bifidum CSUR P1194, Bifidobacterium breve CSUR P7882, Bacteroides ovatus CSUR P4577, Bacteroides uniformis CSUR P2248 and Bacteroides thetaiotaomicron CSUR P7324 were able to inhibit the growth of T. denticola with B. longum being the most efficient.ConclusionsThese results highlight an antagonism between Bifidobacterium species, known probiotics and bio-preservatives, and Treponema spp. This may help to explain the variation of Treponema prevalence in high-income countries and middle- and low-income countries which might linked to the differential consumption of fermented dairy foodstuff and processed food and therefore to the phenomenon of nutrition transition.

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Ecological and evolutionary adaptations shape the gut microbiome of BaAka African rainforest hunter-gatherers

Cited by 4 publications

References 63 publications

Variation in Rural African Gut Microbiota Is Strongly Correlated with Colonization by Entamoeba and Subsistence

Variation in Rural African Gut Microbiota Is Strongly Correlated with Colonization by Entamoeba and Subsistence

Variation in rural African gut microbiota is strongly correlated with colonization byEntamoebaand subsistence

Prevalence of Treponema species in the Gut Microbiome is Linked to Bifidobacterium sp. and Bacteroides sp.

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