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Diet can impact host health through changes to the gut microbiota, yet we lack mechanistic understanding linking nutrient availability and microbiota composition. Here, we use thousands of microbial communities culturedin vitrofrom human feces to uncover simple assembly rules and develop a predictive model of community composition upon addition of single nutrients from central carbon metabolism to a complex medium. Community membership was largely determined by the donor feces, whereas relative abundances were determined by the supplemental carbon source. The absolute abundance of most taxa was independent of the supplementing nutrient, due to the ability of fast-growing organisms to quickly exhaust their niche in the complex medium and then exploit and monopolize the supplemental carbon source. Relative abundances of dominant taxa could be predicted from the nutritional preferences and growth dynamics of species in isolation, and exceptions were consistent with strain-level variation in growth capabilities. Our study reveals that community assembly follows simple rules of nutrient utilization dynamics and provides a predictive framework for manipulating gut commensal communities through nutritional perturbations.

Microbial interactions are expected to modulate microbial diversity, but whether they inhibit or stimulate further diversity in complex microbial communities, and how, remains poorly understood. By assembling microbial communities in multiple identical habitats with a single limiting nutrient, here we provide direct evidence for the role of microbial niche construction and cross-feeding in driving a positive relationship between community diversity and focal lineage diversity in microbial communities. Combining these experiments with simulations, we show that this positive relationship is not inevitable but depends on the underlying metabolic structure of by-product secretions and uptake between different taxonomic levels.

Microbial communities are highly diverse, and understanding the factors that promote and modulate this diversity is a major area of research in microbial ecology. Recent work has proposed a reductionist perspective to microbial coexistence, where pairwise coexistence between strains in isolation is required for their coexistence in a more complex community. In this view, species exclusion in pairwise co-culture would preclude their coexistence in a more complex community too. An alternative view is that coexistence is a more complex property of the entire community, requiring the presence of additional community members. If this view were correct, competitive exclusion in pairwise co-culture would not necessarily preclude species coexistence in more complex community contexts. Empirically testing these alternative hypotheses is complicated by the intractably high microbial diversity of most natural communities, and the challenges of reconstituting every pair of coexisting species under the exact same habitat where their community of origin was assembled. To address this challenge, we have experimentally reconstituted all possible pairwise co-cultures between stably coexisting species from 13 different, low-diversity microbial enrichment communities, which had previously been assembled in a well-controlled synthetic habitat. We find that, when isolated from the rest of their community members, most species pairs fail to coexist. This result highlights the importance of community context for microbial coexistence and indicates that pairwise exclusion may not reflect the ability of species to coexist in more complex, multispecies ecosystems., This work was partially funded by Young Investigator Award RGY0077/2016 from the Human Frontier Science Program (to A.S.). C, C.-Y. was supported by the Graduate Student Fellowship for Studying Abroad from the Ministry of Education, Taiwan.

Summary For microbiome biology to become a more predictive science, we must identify which descriptive features of microbial communities are reproducible and predictable, which are not, and why. We address this question by experimentally studying parallelism and convergence in microbial community assembly in replicate glucose-limited habitats. Here, we show that the previously observed family-level convergence in these habitats reflects a reproducible metabolic organization, where the ratio of the dominant metabolic groups can be explained from a simple resource-partitioning model. In turn, taxonomic divergence among replicate communities arises from multistability in population dynamics. Multistability can also lead to alternative functional states in closed ecosystems but not in metacommunities. Our findings empirically illustrate how the evolutionary conservation of quantitative metabolic traits, multistability, and the inherent stochasticity of population dynamics, may all conspire to generate the patterns of reproducibility and variability at different levels of organization that are commonplace in microbial community assembly.