Worlds within worlds: evolution of the vertebrate gut microbiota

Abstract

In this Analysis we use published 16S ribosomal RNA gene sequences to compare the bacterial assemblages that are associated with humans and other mammals, metazoa and free-living microbial communities that span a range of environments. The composition of the vertebrate gut microbiota is influenced by diet, host morphology and phylogeny, and in this respect the human gut bacterial community is typical of an omnivorous primate. However, the vertebrate gut microbiota is different from free-living communities that are not associated with animal body habitats. We propose that the recently initiated international Human Microbiome Project should strive to include a broad representation of humans, as well as other mammalian and environmental samples, as comparative analyses of microbiotas and their microbiomes are a powerful way to explore the evolutionary history of the biosphere.

Figure 1. Factors shaping the mammalian gut microbiota

Schematic representation of the impact of host phylogeny, gut morphology and diet on fecal bacterial community composition, . A host phylogeny (far left) shows the evolutionary relationships of a representative set of mammals whose names are colored according to diet. The gut morphologies of the mammals are indicated with arrows, as well as their diet categories and the type of fecal bacterial community recovered (Types 1-532). Related animals typically have the same type of gut, diet and gut bacterial community (e.g., the Artiodactyla, green arrows). Other branches of the mammalian tree have `outlier' species, such as the Columbine monkeys in the Primates, whose gut physiology (foregut enlargement) and diet (herbivory) are unusual for the lineage. Note that although sampled animals with simple gut morphologies can have a variety of diets, they only hd community types 3,4 and 5; carnivores only had type 5 fecal bacterial communities, even though type 5 communities were found in animals with a variety of diets.

Figure 2. Variance in bacterial community composition between samples from vertebrate-gut associated and other `free-living' communities

Principal Coordinates Analysis (PCoA) of unweighted UniFrac values, for 464 environmental samples representing 99,801 16S rRNA sequences from free-living and animal-associated environments. Each point represents a sample, colored by habitats. The uppermost panel describes the color codes. The color designations in the middle section refer to all of the panels (A-F). The color designations to the right and left only refer to the panels in their respective columns. All sequences were aligned with NAST and added to the Greengenes core set tree using parsimony insertion in Arb. Near identical sequences were removed from each environmental sample using Divergent Set. Samples with less than 15 divergent sequences in the full dataset (panels A and B), and with less than four divergent sequences within a particular division (panels C-F) were removed from the analysis. (A,B) UniFrac PCoA clustering results for the bacteria, Principal Coordinate (PC) 1 versus PC2 (panel A) and PC1 versus PC3 (panel B). (C-F) PCoA of UniFrac values from selected bacterial phyla including the Bacteroidetes (panels C, D), the Firmicutes (panel E), and the Proteobacteria (panel F). The phylogenetic tree for each phylum was extracted from the same Arb parsimony insertion tree used in panel A. The percent of the variation described by the plotted PC axes are indicated.

Figure 3. Relative abundance of phyla in samples

Bar graph showing the proportion of sequences from each sample that could be classified at the phylum level. The color codes for the dominant Firmicutes as well as the Bacteroidetes phyla are shown. For a complete description of the color codes see Supplementary Figure 1. `Other human' refers to body habitats other than the gut: i.e, mouth, ear, skin, vagina and vulva (see Table S1 for details).

Figure 4. Network analysis of bacterial communities from animal-associated and free-living communities

A simplified cartoon illustration of a host-gut microbe network is shown. In this Figure network diagrams are color-coded by habitat category. Host node colors in (A) highlight the human sample types, while the free-living are the same color. In (B), all vertebrate gut are colored the same, while free-living samples are colored differently from one another. Group abbreviations have the following meaning: VertGut, Vertebrate Gut; HumGut, Human Gut; TermGut, Termite Gut; NonsalInvert, Invertebrate from non-saline environments including diverse insects and earthworms; SalInvert, corals and sponges; HumSkin, Human Skin; HumMouth, Human Mouth; Plant, tightly adherent to plant roots; HumVagina, Human vagina; HumEar, Human Ear.

Figure 5

Network analysis of bacterial communities from animal-associated and free-living communities where host node colors are all white, and genus-level OTUnodes are colored according to their phylogenetic classification at the phylum level.