Habitat Adaptation and Genome Evolution in the Gut Microbiome

We live in a world suffused with microbial life. Universal trees of life show that microbial bacteria, archaea, and eukaryotes constitute the vast majority of life\u27s diversity. These diverse organisms perform many important ecological functions across a wide range of natural and man-made environments: photosynthesis in the world\u27s oceans; nitrogen fixation and provision of carbohydrates in association with plant roots; and modification of the chemistry of the upper atmosphere by microbial communities in droplets of cloud-water. The bodies of animals are also colonized internally and externally by microorganisms, which play crucial roles in the development, homeostasis, and even behavior of their hosts. How have microbial bacteria, archaea, and eukaryotes adapted to survive and thrive across such a range of lifestyles and habitats? I addressed one aspect of this question by using the bacteria inhabiting the mammalian gut as a model for exploring how habitat adaptation impacts the evolution of microbial genomes. I characterized the relationship between 16S rRNA gene sequence similarity and overall levels of gene conservation in the genomes of four groups of species: gut specialists and cosmopolitans, each of which can be divided into pathogens and non-pathogens. At short phylogenetic distances, specialist or cosmopolitan bacteria found in the gut share fewer genes than is typical for genomes that come from non-gut environments, but at longer phylogenetic distances gut bacteria are more similar to each other than are genomes at equivalent evolutionary distances from non-gut environments, suggesting a pattern of short-term specialization but long-term convergence. Moreover, this pattern is observed in both pathogens and non-pathogens, and can even be seen in the plasmids carried by gut bacteria. This observation is consistent with the finding that, despite considerable interpersonal variation in species content, there is surprising functional convergence in the microbiome of different humans. Finally, I observed that even within bacterial species or genera 16S rRNA divergence provides useful information about average conservation of gene content. The results described here should be useful for guiding strain selection to maximize novel gene discovery in large-scale genome sequencing projects, while the approach could be applied in studies seeking to understand the effects of habitat adaptation on genome evolution across other body habitats or environment types