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. 2015 Apr 3;1(3):e1500183.
doi: 10.1126/sciadv.1500183.

The Microbiome of Uncontacted Amerindians

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Free PMC article

The Microbiome of Uncontacted Amerindians

Jose C Clemente et al. Sci Adv. .
Free PMC article

Abstract

Most studies of the human microbiome have focused on westernized people with life-style practices that decrease microbial survival and transmission, or on traditional societies that are currently in transition to westernization. We characterize the fecal, oral, and skin bacterial microbiome and resistome of members of an isolated Yanomami Amerindian village with no documented previous contact with Western people. These Yanomami harbor a microbiome with the highest diversity of bacteria and genetic functions ever reported in a human group. Despite their isolation, presumably for >11,000 years since their ancestors arrived in South America, and no known exposure to antibiotics, they harbor bacteria that carry functional antibiotic resistance (AR) genes, including those that confer resistance to synthetic antibiotics and are syntenic with mobilization elements. These results suggest that westernization significantly affects human microbiome diversity and that functional AR genes appear to be a feature of the human microbiome even in the absence of exposure to commercial antibiotics. AR genes are likely poised for mobilization and enrichment upon exposure to pharmacological levels of antibiotics. Our findings emphasize the need for extensive characterization of the function of the microbiome and resistome in remote nonwesternized populations before globalization of modern practices affects potentially beneficial bacteria harbored in the human body.

Figures

Fig. 1
Fig. 1. Microbiota diversity in fecal, oral, and skin samples from uncontacted Yanomami in relation to other human groups.
(A) Faith’s phylogenetic diversity (PD) (average ± SD) of fecal samples from Yanomami and Guahibo Amerindians, Malawians, and U.S. subjects. OTU tables rarefied at 5000 sequences per sample. Interpopulation differences were significant (P < 0.001, ANOVA with Tukey’s HSD) for all but Guahibo-Malawi comparison (P = 0.73). (B) PCoA plot based on UniFrac distances calculated on the OTU table of fecal samples rarefied at 5000 sequences per sample. (C) Top discriminative bacteria among populations in fecal samples as determined by linear discriminant analysis (LDA) effect size (LEfSe) analysis. (D) Normalized prevalence/abundance curves for all OTUs found at 1% abundance or more in fecal samples. (E) Faith’s phylogenetic diversity (average ± SD) of oral samples from Yanomami and U.S. subjects. OTU tables rarefied at 1500 sequences per sample. Interpopulation differences were not significant (P = 0.296, ANOVA with Tukey’s HSD). (F) PCoA plot based on UniFrac distances calculated on OTU tables of oral samples rarefied at 1500 sequences per sample. (G) Top discriminative bacteria among populations in oral samples as determined by LEfSe analysis. (H) Normalized prevalence/abundance curves for all OTUs found at 1% abundance or more in oral samples. (I) Faith’s phylogenetic diversity (average ± SD) of skin samples from Yanomami and U.S. subjects. OTU tables rarefied at 1500 sequences per sample. Interpopulation differences were significant (P < 0.001, ANOVA with Tukey’s HSD). (J) PCoA plot based on UniFrac distances calculated on OTU tables of skin samples rarefied at 1500 sequences per sample. (K) Top discriminative bacteria among populations in skin samples as determined by LEfSe analysis. (L) Normalized prevalence/abundance curves for all OTUs found at 1% abundance or more in skin samples.
Fig. 2
Fig. 2. Metagenomic diversity of fecal and oral samples from uncontacted Yanomami in relation to other human groups.
(A) Functional diversity (average ± SD) measured by the observed number of KEGG orthologs in fecal samples of Yanomami and Guahibo Amerindians, Malawians, and U.S. subjects. Metagenomic tables rarefied at 1 million sequences per sample. Interpopulation differences were significant for all comparisons (P < 0.001, ANOVA and Tukey’s HSD). (B) PCoA plot based on Bray-Curtis distances calculated on the metagenomic table of fecal samples rarefied at 1 million sequences per sample. (C) Top discriminative metabolic pathways in Yanomami fecal samples as determined by STAMP; pathways ranked by effect size (η2). (D) Normalized prevalence/abundance curves for all KOs found at 1% abundance or more in fecal samples. (E) Functional diversity (average ± SD) measured by the observed number of KEGG orthologs in oral samples of Yanomami and Guahibo Amerindians, Malawians, and U.S. subjects. Metagenomic tables rarefied at 900,000 sequences per sample. Interpopulation differences were not significant (P = 0.07, t test). (F) PCoA plot based on Bray-Curtis distances calculated on the metagenomic table of oral samples rarefied at 900,000 sequences per sample. (G) Top discriminative metabolic pathways in Yanomami oral samples as determined by STAMP; pathways ranked by effect size (η2). (H) Normalized prevalence/abundance curves for all KOs found at 1% abundance or more in oral samples. (I) Functional diversity (average ± SD) measured by the observed number of KEGG orthologs in skin samples of Yanomami and U.S. subjects. Metagenomic tables rarefied at 1 million sequences per sample. Interpopulation differences were significant for all comparisons (P < 0.001, ANOVA and Tukey’s HSD). (J) PCoA plot based on Bray-Curtis distances calculated on the metagenomic table of skin samples rarefied at 1 million sequences per sample. (K) Top discriminative metabolic pathways in Yanomami skin samples as determined by STAMP; pathways ranked by effect size (η2). (L) Normalized prevalence/abundance curves for all KOs found at 1% abundance or more in skin samples.
Fig. 3
Fig. 3. Representative AR genes captured through functional metagenomic selection of Amerindian oral and fecal microbiota.
(A) Maximum likelihood (ML) tree of ceftazidime-resistant PBPs from Amerindian oral microbiota (blue) and their top blastx hits in NCBI nr (black). (B) Identity (%) of the 28 AR genes to their top hits in HMP and MetaHIT (blastn). Fourteen aligned to MetaHIT, all isolated from fecal microbiota. (C) Chloramphenicol acetyltransferase (cat) from O23_CH_21 and homologs in NCBI nt (nucleotide database). Dashed lines indicate 99% identical sequences. Dashes indicate omitted sequence (8487..25716). (D) tetW from F6_TE_1 and homologs in NCBI nt. Dashed lines indicate 98 to 99% identical sequences. Sequences are to scale. Yellow, AR gene; red, other resistance genes; green, mobile genetic elements; purple, bacteriophage genes; blue, other.
Fig. 4
Fig. 4. Abundance of functionally selected AR genes in Amerindian fecal and oral metagenomes.
The heatmap displays the abundances in RPKM (reads per 1-kb gene sequence per million reads mapped) of functionally selected AR genes in the fecal and oral metagenomes of Amerindians. The AR genes were functionally selected from the oral and fecal microbiota of the Yanomami individuals and matched Puerto Rican controls. The shotgun-sequenced metagenomes are from the Yanomami villagers, including individuals not investigated with functional metagenomic selections. Shotgun-sequenced metagenomes were clustered by UPGMA (unweighted pair group method with arithmetic mean) on the AR gene abundance profiles. Fecal and oral microbiota cluster apart.

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