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Worlds within worlds: evolution of the vertebrate gut microbiota

Key Points

  • Comparative analyses between microbial communities in the human gut versus diverse other environments can help elucidate the environmental and evolutionary parameters that shape our intestinal microbiota. Here we use published 16S ribosomal RNA gene sequences to compare the bacterial assemblages that are associated with humans, other mammals, other metazoa and free-living microbial communities that span a range of environmental conditions.

  • Gut microorganisms and their animal hosts have co-evolved, and exploitation of a new diet niche is a powerful driver of the co-evolution of hosts and gut bacteria.

  • Gut microbial communities are distinct from those of other characterized habitats in the biosphere.

  • The vast dichotomy between vertebrate gut and free-living communities is evident from the bacterial phyla that comprise them, which indicates that strong selective forces differentiated gut-dwelling bacteria regardless of their lineage.

  • Most extant mammals are herbivores. The microbial 'solution' to herbivory in mammals with either a simple gut, hindgut or foregut seems to be similar, regardless of host phylogeny: that is, promiscuous gut microorganisms seem to have made it possible for 'unrelated' mammals with similar gut structures to assemble similar microbial communities to digest their polysaccharide-rich diets. This 'bottom-up' perspective of evolution implies that gut microorganisms are unindicted co-conspirators in the spectacular success of mammals.

  • Although few humans have been sampled to date, we seem to be typical omnivores that can be placed together with our omnivorous primate relatives. The recently initiated, international Human Microbiome Project should strive to include a wide representation of humans, as well as other mammals and environmental samples; comparative analyses of microbiotas and their microbiomes are a powerful and timely way to explore the evolutionary history of the biosphere.

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.

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Figure 1: Factors that shape the mammalian gut microbiota.
Figure 2: Variation in bacterial community composition between vertebrate gut-associated and free-living communities.
Figure 3: Relative abundance of phyla in samples.
Figure 4: Network analysis of bacterial communities from animal-associated and free-living communities.
Figure 5: Network analysis of bacterial communities from animal-associated and free-living communities.

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Acknowledgements

Work in the authors' laboratories is supported by grants from the National Institutes of Health (NIH), the National Science Foundation (NSF), the W.M. Keck Foundation and the Crohn's and Colitis Foundation of America. M.H. is supported by training grants from the NIH (grant number T32GM065103) and NSF (East Asia and Pacific Summer Institutes (EAPSI) fellowship number OISE0812861).

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Glossary

Microbiota

The complete set of microbial lineages that live in a particular environment.

Co-evolution

A process in which the evolution of one taxon or trait reciprocally influences the evolution of another.

Co-metabolite

A metabolite that is synthesized or degraded by both the host and one or more microbial species.

Microbiome

The complete collection of genes in the genomes of microorganisms that live in a particular environment (that is, the set of genes contained in a microbiota).

UniFrac

A phylogenetic analysis technique that measures the distance between two community samples in terms of the amount of sequence divergence on a phylogenetic tree that is unique to each of the samples. In practice, a 'master' phylogenetic tree is constructed using all 16S ribosomal RNA sequences from all biological samples characterized in a study. Pairwise comparisons of samples (communities) are then performed with similarity defined (UniFrac metric) based on the degree of branch length that they share on the tree.

Operational taxonomic unit

(OTU). A group of organisms that is defined by its sequence similarity (for Bacteria and Archaea, typically using their 16S ribosomal RNA (rRNA) genes). For example, OTUs at the 97% level (all 16S rRNA gene sequences are at least 97% identical) are often considered to define a species.

OTU-based analysis

An analysis that is based on the counts of each type of OTU in each sample. Unlike phylogenetic analyses, in this approach, all OTUs are considered to be equal, independent units. For example, two OTUs that are closely related to one another will be treated the same as two OTUs that are distantly related.

Horizontal gene transfer

A process by which a gene moves between two genomes rather than being vertically transmitted from parent to offspring.

Principal coordinate analysis

An analysis that is based on a matrix of distances between samples, and detects a few dimensions to explain as much of the variation in the samples as possible using linear algebra techniques.

Co-diversification

A process in which two lineages speciate in concert with one another; for example, when pathogens or commensals speciate into specialist lineages at the same time as their host lineage speciates.

Metagenomics

Culture-independent analyses of the composition and dynamic operations of microbial communities. This includes community characterization at the level of DNA (microbiome), RNA (metatranscriptome), proteins (metaproteome) and metabolic networks (metabolome).

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Ley, R., Lozupone, C., Hamady, M. et al. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6, 776–788 (2008). https://doi.org/10.1038/nrmicro1978

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