Microbial genomes from non-human primate gut metagenomes expand the primate-associated bacterial tree of life with over 1000 novel species

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.

Age-Related Colonic Mucosal Microbiome Community Shifts in Monkeys

“…Consistent with studies on NHPs (35)(36)(37) and humans (4, 5, 7), we also found the gut microbiome was dominated by Bacteroidetes and Firmicutes phyla across the age groups. Similar to a study by Biagi et al (4), we found an overall increase in opportunistic pathobionts such as Proteobacteria phylum, and changes in Bacteroidetes and Firmicutes in old monkeys.…”

“…Human (7,8,40) and NHP (35,37) studies reported prevalence of genera that belong to Prevotellaceae in the gut. Interestingly, members of Prevotellaceae and Helicobacteraceae are known to augment mucosal inflammation enabling dissemination of bacterial products to the systemic circulation (36,37,41). We previously demonstrated associations between increased systemic microbial translocation and innate immune responses impacting metabolic health in aged monkeys (12).…”

Analysis of 1321 Eubacterium rectale genomes from metagenomes uncovers complex phylogeographic population structure and subspecies functional adaptations

“…New technologies and computational tools are generating an unprecedented amount of strain-specific genomic information that can be the foundation of a new generation of microbiome studies [2,12,13,34,35]. Large-scale species-specific whole-genome investigations can now be performed without cultivation [14] and-using metagenomic assembly combined with a reference-dependent binning approach-can be applied on many thousands of single metagenomes.…”

“…In order to find E. rectale genomes assembled from wild non-human primate metagenomes, we assembled and binned as described elsewhere [2,51] a total of 2895 metagenomic high-quality genomes obtained from 175 publicly available metagenomes from wild, nonhuman primates (Additional file 8: Table S7). These 175 metagenomes come from four different datasets spanning 22 non-human primate species including chimpanzees and gorillas from 14 different countries on five continents [45][46][47][48].…”

Precise phylogenetic analysis of microbial isolates and genomes from metagenomes using PhyloPhlAn 3.0

“…We used PhyloPhlAn 3.0 to generate the phylogenies of 1000 S. aureus reference genomes and 135 S. aureus isolates as discussed in the results. To evaluate the phylogeny generated by Phy-loPhlAn 3.0 we used the tqDist 71 function available in the R quartet package to compare quartet distances between the PhyloPhlAn 3.0 and the manually curated reference phylogeny 72 .…”