Indigenous infants in remote Australia retain an ancestral gut microbiome despite encroaching Westernization

Abstract

Studies of traditional Indigenous compared to 'Western' gut microbiomes are underrepresented, and lacking in young children, limiting knowledge of early-life microbiomes in different cultural contexts. Here we analyze the gut metagenomes of 50 Indigenous Australian infants (median age <one year) living remotely with variable access to Western foods, compared to age- and sex-matched non-Indigenous infants living in urban Australia. Indigenous infants had greater alpha diversity and significant differences in bacterial beta diversity, with 114 species and 38 genera differing in abundance. Indigenous infants almost exclusively had higher carriage of Megaspaera, Streptococcus, Caecibacter, Parolsenella and Prevotella species, and markedly higher numbers of gut viruses and fungi. Bifidobacteria ssp. were dominant in Indigenous infants. Despite encroaching Westernisation, the gut microbiome of Indigenous infants retains key features of traditional societies worldwide, attesting to the dominant influence of remote environment and traditional lifestyle in maintaining microbiome diversity.

Fig. 1. Bar charts of observed taxa (bacteria) proportions (25 most abundant) classified by MetaPhlAn.

a Elcho (Indigenous) infants. b ENDIA (Non-indigenous) infants. For each population, samples were ranked left to right by increasing age. Relative proportions of taxa are ranked highest from bottom to top.

Fig. 2. Bar charts of observed taxa (viruses) proportions (25 most abundant) classified by Kraken2.

a Elcho (Indigenous) infants. b ENDIA (Non-indigenous) infants. For each population, samples were ranked left to right by increasing age. Relative proportions of taxa are ranked highest from bottom to top.

Fig. 3. Bar charts of observed taxa (fungi) proportions (25 most abundant) classified by Kraken2.

a Elcho (Indigenous) infants. b ENDIA (Non-indigenous) infants. For each population, samples were ranked left to right by increasing age. Relative proportions of taxa are ranked highest from bottom to top. White columns are samples in which no classified fungi were detected.

Fig. 4. Heatmap of non-fungal eukaryote counts classified by Kraken2.

Highest to lowest abundance is indicated by a red to green gradient.

Fig. 5. Dotplots of alpha diversity (Shannon index) for taxonomic levels found to be significantly different between groups (REML, P < 0.05).

a Population (family); b sex (genus); and c age (species). Elcho (Indigenous) = red dots; ENDIA (non-Indigenous) = blue dots. Vertical lines = 5th–95th percentile; boxes = 25th–75th percentile; horizontal lines = means. The selection of age ranges is described in “Methods.” In (c), pair-wise comparisons between age groups were significant (each P = 0.006), except for 13–149 vs. 160–285 days and 306–441 vs. 458–617 days (P = 1.000). This information is also in Supplementary Data 4.

Fig. 6. Principal coordinate analysis (PCO) plots of beta diversity at the species level.

Each plot is the same PCO with the points colored to indicate different categories or groups. a Population; b sex; c age; PCO1 (x-axis) = 13.3% and PCO2 (y-axis) = 6.7% of total variation. Selection of age ranges is described in “Methods”.

Fig. 7. Differentially abundant taxa between ELCHO and ENDIA infants.

Significantly differentially abundant taxa are shown at the species (a), genus (b) and family (c) levels (ALDEx2 BH  < 0.05) (BH = expected Benjamini–Hochberg-corrected P value of Welch ’s t-test). ALDEx2 was performed using CLR normalization, but the figures depict raw counts. For each taxon, highest to lowest abundance is indicated by red to green gradient. Taxa are sorted by effect size, lowest to highest, top to bottom, i.e., increased abundance in Elcho vs. ENDIA.