Worlds within worlds: evolution of the vertebrate gut microbiota

Abstract

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.