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Cited by 862Gut microbiota and healthAntibiotic Resistance in BacteriaMicrobial Community Ecology and Physiology

The DOI matches its Crossref record; 75 of the 75 references it cites were found in a registry or an index.

The microbiome of uncontacted Amerindians

Open access
Clemente, Jose C., Pehrsson, Erica C., Blaser, Martin J., Sandhu, Kuldip, Gao, Zhan, Wang, Bin, Magris, Magda, Hidalgo, Glida, Contreras, Monica, Noya-Alarcón, Óscar, Lander, Orlana, McDonald, Jeremy, Cox, Mike, Walter, Jens, Oh, Phaik Lyn, Ruiz, Jean F., Rodriguez, Selena, Shen, Nan, Song, Se Jin, Metcalf, Jessica, Knight, Rob, Dantas, Gautam, Dominguez-Bello, M. Gloria·2015·Science Advances
DOI 10.1126/sciadv.1500183PMC PMC4517851
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Abstract

Fecal, oral, and skin biomes of isolated Amerindians show higher human bacterial diversity including antibiotic resistance genes.

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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. 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.CC BY-NC · PubMed Central
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. 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.CC BY-NC · PubMed Central
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. 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.CC BY-NC · PubMed Central
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.
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.CC BY-NC · PubMed Central

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Metadata

Authors
Clemente, J. C., Pehrsson, E. C., Blaser, M. J., Sandhu, K., Gao, Z., Wang, B., Magris, M., Hidalgo, G., Contreras, M., Noya-Alarcón, Ó., Lander, O., McDonald, J., Cox, M., Walter, J., Oh, P. L., Ruiz, J. F., Rodriguez, S., Shen, N., Song, S. J., Metcalf, J., Knight, R., Dantas, G., & Dominguez-Bello, M. G.
Affiliations
  • Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
  • Washington University in St. Louis (US)
  • United States Department of Veterans Affairs (US)
  • New York University (US)
  • Amazonic Center for Research and Control of Tropical Diseases (CAICET), Puerto Ayacucho 7101, Venezuela.
  • Venezuelan Institute for Scientific Research, Caracas 1020-A, Venezuela.
  • Universidad Central de Venezuela (VE)
  • AnMed Health (US)
  • University of Nebraska–Lincoln (US)
  • University of Puerto Rico at Río Piedras (PR)
  • Icahn School of Medicine at Mount Sinai (US)
  • University of Colorado Boulder (US)
  • Howard Hughes Medical Institute (US)
  • New York University School of Medicine, New York, NY 10016, USA.
Corresponding author
  • Pehrsson, Erica C.
  • Sandhu, Kuldip
  • Walter, Jens
  • Knight, Rob
ORCID
Venue
Science Advances
Publisher
American Association for the Advancement of Science (AAAS)
Published
2015-04-03
Volume
1
Issue
3
ISSN
2375-2548 (ISSN-L)
DOI
10.1126/sciadv.1500183
PMC
PMC4517851
OpenAlex
W1986189475
Cited by
851
References
74
Citations by year
2026: 35 · 2025: 55 · 2024: 59 · 2023: 72 · 2022: 81 · 2021: 88 · 2020: 90 · 2019: 103 · 2018: 77 · 2017: 72 · 2016: 86 · 2015: 31
FWCI
38.52
Type
journal article
Language
en
Open access
Licence
cc-by-nc
Locations
  • Science Advances (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • Digital Commons@Becker (Washington University School of Medicine) (submittedVersion)
  • Rutgers University Community Repository (Rutgers University) (submittedVersion)
  • Lincoln (University of Nebraska) (submittedVersion, cc-by-nc)
  • eScholarship (California Digital Library) (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by-nc)
Funders
  • C&D Research Fund (ID0EWFBG929)
  • Emch Research Fund (ID0EBMBG930)
  • NIH SCORE-PES RISE (ID0EMSBG931, 2R25GM061151-13)
  • SUCCESS (ID0EZYBG932)
  • Leona M. and Harry B. Helmsley Charitable Trust (ID0ET1BG933)
  • NIH NIDDK (ID0EN3BG934, DK062429)
  • NAKFI Synthetic Biology (ID0EJ5BG935, SB2, ID0ECAAI936)
  • NIH Director’s New Innovator Award (ID0EYBAI937, NIDDK DP2-DK098089)
  • NIH NIGMS (ID0EQDAI938, R01-GM099538)
  • Washington University I-CARES (ID0EIFAI939)
  • NIH NIAMS (ID0E5GAI940, UH2AR057506)
  • Diane Belfer Program for Human Microbial Ecology (ID0EYIAI941)
  • NDSEG (ID0EQKAI942)
  • Howard Hughes Medical Institute (ID0EEMAI943)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Health Sciences › Medicine › Microbiology (medical) › Antibiotic Resistance in Bacteria
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords
human microbiome, resistome, antibiotic resistance genes, Yanomami, isolated populations, Westernization, bacterial diversity, synthetic antibiotics, gut microbiota, oral microbiota, skin microbiome

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