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Disruption of cross-feeding interactions by invading taxa can cause invasional meltdown in microbial communities.

ABSTRACT: The strength of biotic interactions within an ecological community affects the susceptibility of the community to invasion by introduced taxa. In microbial communities, cross-feeding is a widespread type of biotic interaction that has the potential to affect community assembly and stability. Yet, there is little understanding of how the presence of cross-feeding within a community affects invasion risk. Here, I develop a metabolite-explicit model where native microbial taxa interact through both cross-feeding and competition for metabolites. I use this model to study how the strength of biotic interactions, especially cross-feeding, influence whether an introduced taxon can join the community. I found that stronger cross-feeding and competition led to much lower invasion risk, as both types of biotic interactions lead to greater metabolite scarcity for the invader. I also evaluated the impact of a successful invader on community composition and structure. The effect of invaders on the native community was greatest at intermediate levels of cross-feeding; at this 'critical' level of cross-feeding, successful invaders generally cause decreased diversity, decreased productivity, greater metabolite availability, and decreased quantities of metabolites exchanged among taxa. Furthermore, these changes resulting from a successful primary invader made communities further susceptible to future invaders. The increase in invasion risk was greatest when the network of metabolite exchange between taxa was minimally redundant. Thus, this model demonstrates a case of invasional meltdown that is mediated by initial invaders disrupting the metabolite exchange networks of the native community.

SUBMITTER: Herren CM

PROVIDER: S-EPMC7287355 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Disruption of cross-feeding interactions by invading taxa can cause invasional meltdown in microbial communities.

Herren Cristina M CM

Proceedings. Biological sciences 20200513 1927

The strength of biotic interactions within an ecological community affects the susceptibility of the community to invasion by introduced taxa. In microbial communities, cross-feeding is a widespread type of biotic interaction that has the potential to affect community assembly and stability. Yet, there is little understanding of how the presence of cross-feeding within a community affects invasion risk. Here, I develop a metabolite-explicit model where native microbial taxa interact through both ...[more]

PMID: 32396806

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Project description:BACKGROUND:The species composition of a microbial community is rarely fixed and often experiences fluctuations of varying degrees and at varying frequencies. These perturbations to a community's taxonomic profile naturally also alter the community's functional profile-the aggregate set of genes encoded by community members-ultimately altering the community's overall functional capacities. The magnitude of such functional changes and the specific shift that will occur in each function, however, are strongly dependent on how genes are distributed across community members' genomes. This gene distribution, in turn, is determined by the taxonomic composition of the community and would markedly differ, for example, between communities composed of species with similar genomic content vs. communities composed of species whose genomes encode relatively distinct gene sets. Combined, these observations suggest that community functional robustness to taxonomic perturbations could vary widely across communities with different compositions, yet, to date, a systematic study of the inherent link between community composition and robustness is lacking. RESULTS:In this study, we examined how a community's taxonomic composition influences the robustness of that community's functional profile to taxonomic perturbation (here termed taxa-function robustness) across a wide array of environments. Using a novel simulation-based computational model to quantify this taxa-function robustness in host-associated and non-host-associated communities, we find notable differences in robustness between communities inhabiting different body sites, including significantly higher robustness in gut communities compared to vaginal communities that cannot be attributed solely to differences in species richness. We additionally find between-site differences in the robustness of specific functions, some of which are potentially related to site-specific environmental conditions. These taxa-function robustness differences are most strongly associated with differences in overall functional redundancy, though other aspects of gene distribution also influence taxa-function robustness in certain body environments, and are sufficient to cluster communities by environment. Further analysis revealed a correspondence between our robustness estimates and taxonomic and functional shifts observed across human-associated communities. CONCLUSIONS:Our analysis approach revealed intriguing taxa-function robustness variation across environments and identified features of community and gene distribution that impact robustness. This approach could be further applied for estimating taxa-function robustness in novel communities and for informing the design of synthetic communities with specific robustness requirements.

Project description:BackgroundThe human gut contains approximately 1014 bacteria, belonging to hundreds of different species. Together, these microbial species form a complex food web that can break down nutrient sources that our own digestive enzymes cannot handle, including complex polysaccharides, producing short chain fatty acids and additional metabolites, e.g., vitamin K. Microbial diversity is important for colonic health: Changes in the composition of the microbiota have been associated with inflammatory bowel disease, diabetes, obesity and Crohn's disease, and make the microbiota more vulnerable to infestation by harmful species, e.g., Clostridium difficile. To get a grip on the controlling factors of microbial diversity in the gut, we here propose a multi-scale, spatiotemporal dynamic flux-balance analysis model to study the emergence of metabolic diversity in a spatial gut-like, tubular environment. The model features genome-scale metabolic models (GEM) of microbial populations, resource sharing via extracellular metabolites, and spatial population dynamics and evolution.ResultsIn this model, cross-feeding interactions emerge readily, despite the species' ability to metabolize sugars autonomously. Interestingly, the community requires cross-feeding for producing a realistic set of short-chain fatty acids from an input of glucose, If we let the composition of the microbial subpopulations change during invasion of adjacent space, a complex and stratified microbiota evolves, with subspecies specializing on cross-feeding interactions via a mechanism of compensated trait loss. The microbial diversity and stratification collapse if the flux through the gut is enhanced to mimic diarrhea.ConclusionsIn conclusion, this in silico model is a helpful tool in systems biology to predict and explain the controlling factors of microbial diversity in the gut. It can be extended to include, e.g., complex nutrient sources, and host-microbiota interactions via the intestinal wall.

Project description:We investigated the requirement of 15 human butyrate-producing gut bacterial strains for eight B vitamins and the proteinogenic amino acids by a combination of genome sequence analysis and in vitro growth experiments. The Ruminococcaceae species Faecalibacterium prausnitzii and Subdoligranulum variabile were auxotrophic for most of the vitamins and the amino acid tryptophan. Within the Lachnospiraceae, most species were prototrophic for all amino acids and several vitamins, but biotin auxotrophy was widespread. In addition, most of the strains belonging to Eubacterium rectale and Roseburia spp., but few of the other Lachnospiraceae strains, were auxotrophic for thiamine and folate. Synthetic coculture experiments of five thiamine or folate auxotrophic strains with different prototrophic bacteria in the absence and presence of different vitamin concentrations were carried out. This demonstrated that cross-feeding between bacteria does take place and revealed differences in cross-feeding efficiency between prototrophic strains. Vitamin-independent growth stimulation in coculture compared to monococulture was also observed, in particular for F. prausnitzii A2-165, suggesting that it benefits from the provision of other growth factors from community members. The presence of multiple vitamin auxotrophies in the most abundant butyrate-producing Firmicutes species found in the healthy human colon indicates that these bacteria depend upon vitamins supplied from the diet or via cross-feeding from other members of the microbial community.IMPORTANCE Microbes in the intestinal tract have a strong influence on human health. Their fermentation of dietary nondigestible carbohydrates leads to the formation of health-promoting short-chain fatty acids, including butyrate, which is the main fuel for the colonic wall and has anticarcinogenic and anti-inflammatory properties. A good understanding of the growth requirements of butyrate-producing bacteria is important for the development of efficient strategies to promote these microbes in the gut, especially in cases where their abundance is altered. The demonstration of the inability of several dominant butyrate producers to grow in the absence of certain vitamins confirms the results of previous in silico analyses. Furthermore, establishing that strains prototrophic for thiamine or folate (butyrate producers and non-butyrate producers) were able to stimulate growth and affect the composition of auxotrophic synthetic communities suggests that the provision of prototrophic bacteria that are efficient cross feeders may stimulate butyrate-producing bacteria under certain in vivo conditions.

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Disruption of cross-feeding interactions by invading taxa can cause invasional meltdown in microbial communities.

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Disruption of cross-feeding interactions by invading taxa can cause invasional meltdown in microbial communities.

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