using-single-worm-data-to-quantify-heterogeneity-caenorhabditis

Using Single-Worm Data to Quantify Heterogeneity in <em>Caenorhabditis elegans</em>-Bacterial Interactions

The nematode Caenorhabditis elegans is a model system for host-microbe and host-microbiome interactions. Many studies to date use batch digests rather ...

Emory University

There is a great deal of interest in discovering the principles that organize microbial communities, to better understand the structure and diversity of these communities in the natural world. Recent conceptual and technical advances have shown how simple organizing principles can give rise to surprising diversity and complex patterns in these consortia. Understanding competition, cooperation, and communication among microbes has provided novel insights into the structure and behavior of microbial collectives, and the use of simple animal models has advanced our understanding of microbial ecology in the host. These multidisciplinary efforts to understand and predict the properties of microbial communities will be critical in the development of microbial ecology as an applied science.

Simple organizing principles in microbial communities.

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.

Interspecies bacterial competition regulates community assembly in the C. elegans intestine.

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  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. Here, we used a  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.

Article	Year
Simple organizing principles in microbial communities. Current opinion in microbiology\| PubMed ID: 30503875	2018
Interspecies bacterial competition regulates community assembly in the C. elegans intestine. The ISME journal\| PubMed ID: 33589765	2021
Host Immunity Alters Community Ecology and Stability of the Microbiome in a Caenorhabditis elegans Model. mSystems\| PubMed ID: 33879498	2021
From a parts list to assembly instructions and an operating manual: how small host models can re-write microbiome theory. Current opinion in microbiology\| PubMed ID: 34739919	2021

Nic M. Vega

Biography

JoVE Journal Publications

Other Publications