Communities of microbial eukaryotes in the mammalian gut within the context of environmental eukaryotic diversity

Abstract

Eukaryotic microbes (protists) residing in the vertebrate gut influence host health and disease, but their diversity and distribution in healthy hosts is poorly understood. Protists found in the gut are typically considered parasites, but many are commensal and some are beneficial. Further, the hygiene hypothesis predicts that association with our co-evolved microbial symbionts may be important to overall health. It is therefore imperative that we understand the normal diversity of our eukaryotic gut microbiota to test for such effects and avoid eliminating commensal organisms. We assembled a dataset of healthy individuals from two populations, one with traditional, agrarian lifestyles and a second with modern, westernized lifestyles, and characterized the human eukaryotic microbiota via high-throughput sequencing. To place the human gut microbiota within a broader context our dataset also includes gut samples from diverse mammals and samples from other aquatic and terrestrial environments. We curated the SILVA ribosomal database to reflect current knowledge of eukaryotic taxonomy and employ it as a phylogenetic framework to compare eukaryotic diversity across environment. We show that adults from the non-western population harbor a diverse community of protists, and diversity in the human gut is comparable to that in other mammals. However, the eukaryotic microbiota of the western population appears depauperate. The distribution of symbionts found in mammals reflects both host phylogeny and diet. Eukaryotic microbiota in the gut are less diverse and more patchily distributed than bacteria. More broadly, we show that eukaryotic communities in the gut are less diverse than in aquatic and terrestrial habitats, and few taxa are shared across habitat types, and diversity patterns of eukaryotes are correlated with those observed for bacteria. These results outline the distribution and diversity of microbial eukaryotic communities in the mammalian gut and across environments.

Keywords: host-associated eukaryotes; human microbiome; intestinal protozoa; microbial diversity; microbial ecology; parasites; protist; salinity.

Figure 1

Relative taxon abundance of mammalian (including human) fecal samples demonstrates heterogeneity in the presence of eukaryotic lineages across mammals, while the same bacterial lineages are consistently dominant. (A) Eukaryotes, (B) bacteria. Each bar represents an individual fecal sample from humans and other mammals, and only samples with at least 150 sequences in the 18S are represented.

Figure 2

Comparison of the phylogenetic distribution of taxa from mammalian gut to other environments. Sequences detected in the mammalian gut come from a smaller number of lineages and have lower overall diversity compared to other environments, reflecting the limited number of lineages that have successfully colonized animal hosts. Tree contains sequences from 32 mammalian gut samples (red) and 32 samples total from skin, terrestrial, and aquatic habitats (blue). Tips present correspond to the data rarefied to 150 sequences per sample for comparison. (A) Eukaryotic 18S rRNA tree constructed using RAxML with the topology constrained to the SILVA 108 reference tree. (B) Bacterial 16S rRNA tree from Greengenes 2011 release. Branches are colored according to the environment that contributed the majority of the sequences.

Figure 3

Bar chart of the relative abundance of sequences falling into the major clades of eukaryotes depicts the overall divergence in community composition across sample types. Major clades are the deepest divisions within eukaryotes (Parfrey et al., ; Adl et al., 2012) and are roughly equal to the phyla or superphyla level of bacteria.

Figure 4

NMDS plot of unweighted UniFrac reveal separation across major environmental categories. Plots (A) Eukaryotes and (B) Bacteria show the distinction between fecal samples (red and orange) and those from other environments, including skin (pink). Air samples were collected over terrestrial habitats.