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Vega, N. M.

Publications and source records attributed to Vega, N. M..

7 recordsLinked to original sources

Correlations in microbial abundance data reveal host-bacteria and bacteria-bacteria interactions jointly shaping the C. elegans microbiome

Compositional structure of host-associated microbiomes is potentially affected by interactions among the microbes and between the microbes and the host. To quantify the relative importance of these contributions to the microbiome composition and variation, here we analyze absolute abundance (count) data for a minimal eight-species native microbiome in the Caenorhabditis elegans intestine. We find that a simple neutral model only considering migration, birth, death, and competition for space among the bacteria can capture the means and variances of bacterial abundance, but not the experimental bacteria-bacteria covariances. We find that either bacteria-bacteria interactions or correlations among bacterial population dynamics parameters induced by the host can qualitatively recapitulate the observed correlations among bacterial taxa. However, neither model is uniquely or completely sufficient to explain the data. Further, we observe that different interactions are required to explain (co)variance data in microbiota associated with different host genotypes, suggesting different community dynamics associated with these host types. Finally, we find that many of these signals are obscured when data are converted to proportions from counts, consistent with a growing literature on the limitations of compositional data for inference of population dynamics. We end with discussing the limitations of Lotka-Volterra type assumptions for microbial community data analysis revealed by our results.

biophysics↗

Heterogeneous shedding and susceptibility in a Caenorhabditis elegans transmission model

Variation in transmission plays a crucial role in shaping the dynamics of infectious diseases. Population heterogeneity is known to contribute to this variation and is often represented in epidemiological models. However, it is not always clear a priori what sources of variation should contribute meaningfully to a given scenario, and it can be challenging to infer distributions of underlying processes from data. In this study, we demonstrate the use of Caenorhabditis elegans as a tractable system in which high-quality data can be produced for experimental epidemics. We show that distributions of shedding and susceptibility in this host can be experimentally decoupled to measure heterogeneity in transmission processes. We observe and quantify super-shedding and heterogeneous susceptibility, and we show that distributions of population heterogeneity and transmission outcomes have features conserved with real-world epidemics. Our results quantify sources of heterogeneity in bacterial transmission in this small model organism and establish C. elegans as a promising quantitative model for experimental epidemics.

microbiology↗

A strong priority effect in the assembly of a specialized insect-microbe symbiosis

Microbial community assembly is determined in part by interactions between taxa that colonize ecological niches available within habitat patches. The outcomes of these interactions, and by extension the trajectory of community assembly, can display priority effects - dependency on the order in which taxa first occupy these niches. The underlying mechanisms of these phenomena vary from system to system and are often not well resolved. Here, we characterize priority effects in colonization of the squash bug (Anasa tristis) by bacterial symbionts from the genus Caballeronia, using pairs of strains that are known to strongly compete during host colonization, as well as strains that are isogenic and thus functionally identical. By introducing symbiont strains into individual bugs in a sequential manner, we show that within-host populations established by the first colonist are extremely resistant to invasion, regardless of strain identity and competitive interactions. By knocking down the population of an initial colonist with antibiotics, we further show that colonization success by the second symbiont is still diminished even when space in the symbiotic organ is available and physically accessible for colonization. We propose a paradigm in which resident symbionts exclude subsequent infections by manipulating the host environment, partially but not exclusively by eliciting tissue remodeling of the symbiont organ. ImportanceHost-associated microbial communities underpin critical ecosystem processes and human health, and their ability to do so is determined in turn by the various processes that shape their composition. While natural selection acts on competing genotypes and species during community assembly, the manner by which selection determines the trajectory of community assembly can differ depending on the sequence by which taxa establish within that community. We document this phenomenon, known as a priority effect, during experimental colonization of a North American insect pest, the squash bug Anasa tristis, by its betaproteobacterial symbionts in the genus Caballeronia. Our study demonstrates how stark, strain-level variation can emerge in specialized host-microbe symbioses simply through differences in the order by which strains colonize the host. Understanding the mechanistic drivers of community structure in host-associated microbiomes can highlight both pitfalls and opportunities for the engineering of these communities and their constituent taxa for societal benefit.

microbiology↗

Ecological drift during colonization drives within- and between-host heterogeneity in animal symbiont populations

Host-associated microbiomes vary greatly in composition both within and between host individuals, providing the raw material for natural selection to act on host-microbe associations. Nonetheless, the drivers of compositional heterogeneity in host-associated microbiomes have only rarely been examined. To understand how this heterogeneity arises, we utilize the squash bug, Anasa tristis, and its bacterial symbionts in the genus Caballeronia. We artificially modulate symbiont bottleneck size and strain diversity during colonization to demonstrate the significance of ecological drift, which causes stochastic fluctuations in community composition. Consistent with predictions from the neutral theory of biodiversity, ecological drift alone can account for heterogeneity in symbiont community composition between hosts, even when two strains are nearly genetically identical. When acting on competing, unrelated strains, ecological drift can maintain symbiont genetic diversity among different hosts by stochastically determining the dominant strain within each host. Finally, ecological drift mediates heterogeneity in isogenic symbiont populations even within a single host, along a consistent gradient running the anterior-posterior axis of the symbiotic organ. Our results demonstrate that symbiont population structure across scales does not necessarily require host-mediated selection, but emerges as a result of ecological drift acting on both isogenic and unrelated competitors. Our findings illuminate the processes that might affect symbiont transmission, coinfection, and population structure in nature, which can drive the evolution of host-microbe symbiosis and microbe-microbe interactions within host-associated microbiomes.

microbiology↗

Host immunity alters successional ecology and stability of the microbiome in a C. elegans model

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.

microbiology↗

Colonization with heterologous bacteria reprograms a Caenorhabditis elegans nutritional phenotype

Animals rely on the gut microbiome to process complex food compounds that the host cannot digest and to synthesize nutrients that the host cannot produce. New systems are needed to study how the expanded metabolic capacity provided by the gut microbiome impacts the nutritional status and health of the host. 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. The nutritional benefits of colonization with cellulolytic bacteria were assayed directly, by incorporation of isotopic biomass, and indirectly, as host larval yield resulting from glucose release in the gut. As a community component in the worm gut, cellulolytic bacteria can also support additional bacterial species with specialized roles, which we demonstrate by using Lactobacillus to protect against Salmonella infection. As a model system, C. elegans colonized with cellulolytic bacteria can be used to study microbiome-host interactions. Engineered microbiome communities may provide host organisms with novel functions, such as the ability to use more complex nutrient sources and to fight against pathogen infections. One Sentence SummaryHeterologous bacteria colonizing an animal gut help digest complex sugars to provide nutrition for the host in a model system.

microbiology↗

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

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. However, the complexity of these gut microbiomes and their hosts often constrains our ability to understand how these bacterial communities assemble and function. In order to elucidate basic principles of community assembly in a host intestine, we study the assembly of the microbiome of Caenorhabditis elegans with a bottom-up approach. We colonize the gut of the worm C. elegans with 11 bacterial species individually, in all possible pairs, and in selected trios, and we find an organized mixture of coexistence and competitive exclusion that indicates a hierarchical structure in the bacterial interactions. The capacity of a bacterial species fed in monoculture to colonize the C. elegans intestine correlates with its average fraction in co-culture experiments, yet fails to predict its abundance in many two- and three-species microbiomes. Hence, the bacterial fractional abundances in co-culture experiments--pairwise outcomes--are influenced by interspecies interactions. These pairwise outcomes accurately predict the trio outcomes in the worm intestine, further highlighting the importance of pairwise interactions in determining community composition. We also find that the C. elegans gut environment influences the outcome of co-culture experiments, and demonstrate that the low intestinal pH is one of the causes. These results highlight that a bottom-up approach to microbiome community assembly may provide valuable insight into the structure and composition of complex microbial communities.

microbiology↗