Abstract
BackgroundHumans have coevolved with microbial communities to establish a mutually advantageous relationship that is still poorly characterized and can provide a better understanding of the human microbiome. Comparative metagenomic analysis of human and non-human primate (NHP) microbiomes offers a promising approach to study this symbiosis. Very few microbial species have been characterized in NHP microbiomes due to their poor representation in the available cataloged microbial diversity, thus limiting the potential of such comparative approaches.ResultsWe reconstruct over 1000 previously uncharacterized microbial species from 6 available NHP metagenomic cohorts, resulting in an increase of the mappable fraction of metagenomic reads by 600%. These novel species highlight that almost 90% of the microbial diversity associated with NHPs has been overlooked. Comparative analysis of this new catalog of taxa with the collection of over 150,000 genomes from human metagenomes points at a limited species-level overlap, with only 20% of microbial candidate species in NHPs also found in the human microbiome. This overlap occurs mainly between NHPs and non-Westernized human populations and NHPs living in captivity, suggesting that host lifestyle plays a role comparable to host speciation in shaping the primate intestinal microbiome. Several NHP-specific species are phylogenetically related to human-associated microbes, such as Elusimicrobia and Treponema, and could be the consequence of host-dependent evolutionary trajectories.ConclusionsThe newly reconstructed species greatly expand the microbial diversity associated with NHPs, thus enabling better interrogation of the primate microbiome and empowering in-depth human and non-human comparative and co-diversification studies.
Highlights
Humans have coevolved with microbial communities to establish a mutually advantageous relationship that is still poorly characterized and can provide a better understanding of the human microbiome
Among the functions associated with non-human primate (NHP) strains, we found different genes involved in the degradation of sugars like cellobiose (K00702, K02761) and maltose (K16211, K01232), and among those associated with human ones, genes encoding for the degradation of different antibiotic compounds, including penicillin and vancomycin (K01710, K02563, K07260, K07259), which is consistent with the exposure of humans but not NHPs to antibiotics
In this study, we expanded the fraction of characterized microbial diversity in the highly unexplored non-human primate metagenome, to enable species- and strain-level comparative genomics analysis of the human and nonhuman primate microbiome and generate hypotheses on relevant coevolutionary trajectories that shaped the current worldwide structure of the human microbiome
Summary
Humans have coevolved with microbial communities to establish a mutually advantageous relationship that is still poorly characterized and can provide a better understanding of the human microbiome. Comparative metagenomic analysis of human and non-human primate (NHP) microbiomes offers a promising approach to study this symbiosis. It is difficult to establish causality and mechanisms for these links [15, 16], recent studies have extended the identifiable members of the human microbiome to cover > 90% of its overall diversity [11], which is a prerequisite for advancing the understanding of the role of microbes in human physiology and metabolism. A very substantial fraction of the microbiome in NHPs is currently uncharacterized, and a comprehensive comparative sequencelevel analysis against human microbiomes is unfeasible
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