From insects to mammals, a large variety of animals hold in their intestines complex bacterial communities that play an important role in health and disease. To further our understanding of how intestinal bacterial communities assemble and function, we study the C. elegans microbiota with a bottom-up approach by feeding this nematode with bacterial monocultures as well as mixtures of two to eight bacterial species. We find that bacteria colonizing well in monoculture do not always do well in co-cultures due to interspecies bacterial interactions. Moreover, as community diversity increases, the ability to colonize the worm gut in monoculture becomes less important than interspecies interactions for determining community assembly. To explore the role of host–microbe adaptation, we compare bacteria isolated from C. elegans intestines and non-native isolates, and we find that the success of colonization is determined more by a species’ taxonomy than by the isolation source. Lastly, by comparing the assembled microbiotas in two C. elegans mutants, we find that innate immunity via the p38 MAPK pathway decreases bacterial abundances yet has little influence on microbiota composition. These results highlight that bacterial interspecies interactions, more so than host–microbe adaptation or gut environmental filtering, play a dominant role in the assembly of the C. elegans microbiota.
Microbiomes often form specific functional associations with their hosts. Correlations between microbiome membership and states of host health and disease abound in many systems. However, there are few systems that allow for in depth functional studies that include precise manipulation and interrogation of both microbiome composition and host function. Recently the nematode Caenorhabditis elegans - an excellent genetic model organism for studying many fields of biology, including neurobiology and behavior, development, cell biology, and innate immunity - has proven to be a robust system to probe microbiome interactions and their effect on host physiology.
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 affect 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 analyzed 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 concluded that fundamental differences in microbiome ecology underlie the observed differences in microbiome composition. We tested this hypothesis by introducing a minor perturbation into 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 interspecies interactions within the microbiome, resulting in differences in community composition and stability that emerge from these differences in host-microbe ecology.
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.
Understanding how microbes adapt to their host is an enduring problem in microbiome ecology, and understanding the microbial traits that allow colonization of the host and increase adaptation to the host environment is of particular interest. In this study, Robinson and colleagues use experimental evolution to demonstrate adaptation of a commensal bacterium to its zebrafish host and describe the changes in phenotype that emerge during this evolutionary process. These results provide insight into the evolutionary problem of host adaptation and demonstrate the utility of simple models for understanding host–microbiome dynamics.