Here, we used a Caenorhabditis elegans microbiome model to demonstrate how genetic differences in innate immunity alter microbiome composition, diversity, and stability by changing the ecological processes that shape these communities. These results provide insight into the role of host genetics in controlling the ecology of the host-associated microbiota, resulting in differences in community composition, successional trajectories, and response to perturbation.

Adaptation of replicate microbial communities frequently produces shared trajectories of community composition and structure. However, divergent adaptation of individual community members can occur and is associated with community-level divergence. The extent to which community-based adaptation of microbes should be convergent when community members are similar but not identical is therefore not well understood. In these experiments, adaptation of combinatorial minimal communities of bacteria with the model host Caenorhabditis elegans produces structurally similar communities over time, but with divergent adaptation of member taxa and differences in community-level resistance to invasion. These results indicate that community-based adaptation from taxonomically similar starting points can produce compositionally similar communities that differ in traits of member taxa and in ecological properties.

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The gut microbiome is essential for processing complex food compounds and synthesizing nutrients that the host cannot digest or produce, respectively. New model systems are needed to study how the metabolic capacity provided by the gut microbiome impacts the nutritional status of the host, and to explore possibilities for altering host metabolic capacity via the microbiome. Here, we colonized the nematode Caenorhabditis elegans gut with cellulolytic bacteria that enabled C. elegans to utilize cellulose, an otherwise indigestible substrate, as a carbon source. Cellulolytic bacteria as a community component in the worm gut can also support additional bacterial species with specialized roles, which we demonstrate by using Lactobacillus plantarum to protect C. elegans against Salmonella enterica infection. This work shows that engineered microbiome communities can be used to endow host organisms with novel functions, such as the ability to utilize alternate nutrient sources or to better fight pathogenic bacteria.

A growing body of data suggests that the microbiome of a species can vary considerably from individual to individual, but the reasons for this variation - and the consequences for the ecology of these communities – remain only partially explained. In mammals, the emerging picture is that the metabolic state and immune system status of the host affects the composition of the microbiome, but quantitative ecological microbiome studies are challenging to perform in higher organisms. Here we show that these phenomena can be quantitatively analyzed in the tractable nematode host Caenorhabditis elegans. Mutants in innate immunity, in particular the DAF-2/Insulin Growth Factor (IGF) pathway, are shown to contain a microbiome that differs from that of wild type nematodes. We analyze the underlying basis of these differences from the perspective of community ecology by comparing experimental observations to the predictions of a neutral sampling model and conclude that fundamental differences in microbiome ecology underlie the observed differences in microbiome composition. We test this hypothesis by introducing a minor perturbation to the colonization conditions, allowing us to assess stability of communities in different host strains. Our results show that altering host immunity changes the importance of inter-species interactions within the microbiome, resulting in differences in community composition and stability that emerge from these differences in host-microbe ecology.ImportanceHere we use a Caenorhabditis elegans microbiome model to demonstrate how genetic differences in innate immunity alter microbiome composition, diversity, and stability by changing the ecological processes that shape these communities. These results provide insight into the role of host genetics in controlling the ecology of host-associated microbiota, resulting in differences in community composition, successional trajectories, and response to perturbation.