Gut microbiome of the Hadza hunter-gatherers

Abstract

Human gut microbiota directly influences health and provides an extra means of adaptive potential to different lifestyles. To explore variation in gut microbiota and to understand how these bacteria may have co-evolved with humans, here we investigate the phylogenetic diversity and metabolite production of the gut microbiota from a community of human hunter-gatherers, the Hadza of Tanzania. We show that the Hadza have higher levels of microbial richness and biodiversity than Italian urban controls. Further comparisons with two rural farming African groups illustrate other features unique to Hadza that can be linked to a foraging lifestyle. These include absence of Bifidobacterium and differences in microbial composition between the sexes that probably reflect sexual division of labour. Furthermore, enrichment in Prevotella, Treponema and unclassified Bacteroidetes, as well as a peculiar arrangement of Clostridiales taxa, may enhance the Hadza's ability to digest and extract valuable nutrition from fibrous plant foods.

Figure 1. Location and scenery of Hadza land in Tanzania, Africa.

In deep bush camps, hunting and gathering still make up the majority (>90%) of subsistence. (a) Location of Hadza land in northern Tanzania; (b) top of a rock ridge near Sengele camp overlooking a lush landscape in between two phases of the rainy season; (c) extent of the land surrounding Lake Eyasi where Hadza make their camp sites, orange border denotes land area in 1950s and area in yellow shows the reduced area Hadza occupy today; (d) view of baobab trees within Hadza land during the early dry season. Photo a modified from the CIA World Factbook. Photos b and d by SL Schnorr and AN Crittenden.

Figure 2. Bacterial relative abundance of Hadza and Italian subjects.

16S rDNA gene survey of the faecal microbiota of 27 Hadza (H1-H27) and 16 Italian (IT1-IT16) adults. Relative abundance of (a) phylum and (b) genus-classified faecal microbiota is reported. Histograms are based on the proportion of OTUs per subject. Colours were assigned for all phyla detected, and for genera with a relative abundance ≥1% in at least 10% of subjects. (c) Donut charts summarizing genera relative abundance for Italians (outer donut) and Hadza (inner donut). Genera were filtered for those with ≥2% of total abundance in at least 10% of subjects. *denotes unclassified OTU reported at higher taxonomic level.

Figure 3. Sex difference in GM structure among Hadza and Italians.

PCoAs based on unweighted and weighted UniFrac distances as well as Euclidean and Bray–Curtis distances show patterns of separation by sex within each subject cohort and their respective P-values. Significance was calculated by permutation test with pseudo F-ratio. Pink, females; blue, males.

Figure 4. GM phylogenetic difference between Hadza and Italian subjects.

(a) Unweighted and weighted UniFrac distance PCoA of the faecal microbiota from 27 Hadza (orange dots) and 16 Italians (blue dots). (b) Hierarchical Ward-linkage clustering based on the Spearman correlation coefficients of genus proportion. Genera were filtered for subject prevalence of at least 30% within a population. Subjects are clustered on top of the panel and colour-coded as in a. Genera (110) clustered by the vertical tree are colour coded by family assignment. * denotes unclassified OTU reported at higher taxonomic level.

Figure 5. Comparison of GM relative abundance among populations reflects subsistence patterns.

(a) Hierarchical clustering based on Eisen’s formula of correlation similarity metric of bacterial genus proportion and average linkage clustering. Genera were filtered for subject prevalence of at least 30% of samples. Subjects are clustered in the top of panel and colour-coded orange (Hadza), brown (BF), red (Malawi), blue (Italian adult controls from this study), green (US adults from ref. 9) and cyan (Italian children from ref. 4). Genera (107) are visualized and clustered by the vertical tree. (b) PCoA based on Bray–Curtis distances of the relative abundance of GM genera of each population.

Figure 6. Distinct bacterial co-abundance groups (CAGs) define each population.

Wiggum plots indicate pattern of variation of the six identified CAGs in Hadza, Malawi, BF and western controls. CAGs are named with the name of the most abundant genera and are colour coded as follows: Faecalibacterium (cyan), Dialister (green), Prevotella (orange), Clostridiales_unclassified (yellow), Ruminococcaceae_unclassified (pink) and Blautia (violet). Each node represents a bacterial genus and its dimension is proportional to the mean relative abundance within the population. Connections between nodes represent positive and significant Kendall correlation between genera (FDR<0.05).

Figure 7. Comparison of metabolite production between Hadza and Italian samples.

PCoA based on Euclidean distances of the profiles of SCFA relative abundance in Hadza (orange) and Italians (blue). Vectors show propionate, butyrate and acetate abundance.