The microbiome and resistome of chimpanzees, gorillas, and humans across host lifestyle and geography

Abstract

The gut microbiome can vary across differences in host lifestyle, geography, and host species. By comparing closely related host species across varying lifestyles and geography, we can evaluate the relative contributions of these factors in structuring the composition and functions of the microbiome. Here we show that the gut microbial taxa, microbial gene family composition, and resistomes of great apes and humans are more related by host lifestyle than geography. We show that captive chimpanzees and gorillas are enriched for microbial genera commonly found in non-Westernized humans. Captive ape microbiomes also had up to ~34-fold higher abundance and up to ~5-fold higher richness of all antibiotic resistance genes compared with wild apes. Through functional metagenomics, we identified a number of novel antibiotic resistance genes, including a gene conferring resistance to colistin, an antibiotic of last resort. Finally, by comparing our study cohorts to human and ape gut microbiomes from a diverse range of environments and lifestyles, we find that the influence of host lifestyle is robust to various geographic locations.

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Fig. 1: Taxonomic composition of the human, chimpanzee, and gorilla gut microbiomes.
Fig. 2: Gene family and functional pathway analysis of gut microbiota.
Fig. 3: The antibiotic resistome of humans, chimpanzees, and gorillas.
Fig. 4: Comparison of chimpanzee and gorilla microbiomes to human microbiomes across a wide range of lifestyles and environments.

Data availability

16S rRNA and shotgun metagenomic Illumina sequencing data of human, chimpanzee, and gorilla samples are available from the Sequence Read Archive (SRA) under accession PRJNA539933. 16S rRNA data are de-multiplexed and trimmed. Shotgun metagenomic data are de-multiplexed, trimmed, quality-filtered, and host reads have been removed. Protein sequences of ARGs identified through functional metagenomic selections are available from the National Center for Biotechnology Information under accessions MK935708–MK936039. The colistin resistance gene CL H8 is available under accession MK936039. Counts tables and LEfSe output tables are available in the supplemental spreadsheets.

Code availability

No custom codes or mathematical algorithms were used that are central to the conclusions.

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Acknowledgements

We thank Dr Kenneth Cameroon, Wildlife Conservation Society-Congo Program for assistance in the field and shipping of samples from Congo to the USA. Dr Steve Ross, Maureen Leahy, and the Lester E. Fisher Center great ape staff at Lincoln Park Zoo for their assistance in providing captive ape samples. At the St. Louis Zoo we would like to thank Heidi Helmuth, Jane Merkel, and the great ape care staff. We thank Douglas Berg, Pablo Tsukayama, and Sanket Patel for early discussions regarding study design, and members of the Dantas lab for helpful discussions of the results and paper. This work was supported in part by awards from the National Institutes of Health (NIH) Director’s New Innovator Award, the National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK) of the NIH, and the National Institute of Allergy and Infectious Diseases (NIAID) of the NIH under award numbers DP2DK098089 and R01AI123394 to GD, the Mallinckrodt Scholar Award of the Edward Mallinckrodt Jr. Foundation to GD, and the International Center for Energy, Environment, and Sustainability (InCEES) at Washington University in St Louis to CS. The content is solely the responsibility of the authors and does not necessarily represent the official views of the funding agencies.

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TPC, XS, GD, DM, and CS designed the study and experiments. DM and CS collected samples. TPC, XS, and VHP performed the experiments. TPC analyzed the results. TPC, GD, DM, and CS wrote the paper.

Correspondence to Gautam Dantas.

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Campbell, T.P., Sun, X., Patel, V.H. et al. The microbiome and resistome of chimpanzees, gorillas, and humans across host lifestyle and geography. ISME J (2020). https://doi.org/10.1038/s41396-020-0634-2

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