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Interactions between strains govern the eco-evolutionary dynamics of microbial communities

Video Abstract (AI generated) Paper Preprint Supplementary Material Supplementary Table S1 Supplementary Table S2

Genomic data has revealed that genotypic variants of the same species, i.e., strains, coexist and are abundant in natural microbial communities. However, it is not clear if strains are ecologically equivalent, or if they exhibit distinct interactions and dynamics. Here, we address this problem by tracking 10 microbial communities from the pitcher plant Sarracenia purpurea in the laboratory for more than 300 generations. Using metagenomic sequencing, we reconstruct their dynamics over time and across scales, from distant phyla to closely related genotypes. We find that interactions between naturally occurring strains govern eco-evolutionary dynamics. Surprisingly, even fine-scale variants differing only by 100 base pairs can exhibit vastly different dynamics. We show that these differences may stem from ecological interactions in the communities, which are specific to strains, not species. Finally, by analyzing genomic differences between strains, we identify major functional hubs such as transporters, regulators, and carbohydrate-catabolizing enzymes, which might be the basis for strain-specific interactions. Our work shows that strains are the relevant level of diversity at which to study the long-term dynamics of microbiomes.

Multiple stable states in microbial communities explained by the stable marriage problem

The ISME Journal, 2018-07-19

Video Abstract (AI generated) Paper Preprint The ISME Journal

Experimental studies of microbial communities routinely reveal that they have multiple stable states. While each of these states is generally resilient, certain perturbations such as antibiotics, probiotics and diet shifts, result in transitions to other states. Can we reliably both predict such stable states as well as direct and control transitions between them? Here we present a new conceptual model — inspired by the stable marriage problem in game theory and economics — in which microbial communities naturally exhibit multiple stable states, each state with a different species' abundance profile. Our model's core ingredient is that microbes utilize nutrients one at a time while competing with each other. Using only two ranked tables, one with microbes' nutrient preferences and one with their competitive abilities, we can determine all possible stable states as well as predict inter-state transitions, triggered by the removal or addition of a specific nutrient or microbe. Further, using an example of 7 Bacteroides species common to the human gut utilizing 9 polysaccharides, we predict that mutual complementarity in nutrient preferences enables these species to coexist at high abundances.

Metabolic adaptations underlying genome flexibility in prokaryotes

PLOS Genetics, 2018-10-29

Video Abstract (AI generated) Paper Preprint PLOS Genetics

Even across genomes of the same species, prokaryotes exhibit remarkable flexibility in gene content. We do not know whether this flexible or "accessory" content is mostly neutral or adaptive, largely due to the lack of explicit analyses of accessory gene function. Here, across 96 diverse prokaryotic species, we show that a considerable fraction (~40%) of accessory genomes harbours beneficial metabolic functions. These functions take two forms: (1) they significantly expand the biosynthetic potential of individual strains, and (2) they help reduce strain-specific metabolic auxotrophies via intra-species metabolic exchanges. We find that the potential of both these functions increases with increasing genome flexibility. Together, our results are consistent with a significant adaptive role for prokaryotic pangenomes.

Complementary resource preferences spontaneously emerge in diauxic microbial communities

Video Abstract (AI generated) Paper Preprint Supplementary text and figures (github,"")

Most microbes grow diauxically, utilizing the available resources one at a time rather than simultaneously. The properties of communities of microbes growing diauxically remain poorly understood, largely due to a lack of theory and models of such communities. Here, we develop and study a minimal model of diauxic microbial communities assembling in a serially diluted culture. We find that community assembly repeatably and spontaneously leads to communities with complementary resource preferences i.e., communities where species prefer different resources as their top choice. Simulations and theory explain that the emergence of complementarity is driven by the disproportionate contribution of the top choice resource to the growth of a species. Additionally, we develop a geometric approach for analyzing serially diluted communities, with or without diauxie, which intuitively explains several additional emergent community properties, such as the apparent lack of species which grow fastest on a resource other than their most preferred resource. Overall, our work provides testable predictions for the assembly of natural as well as synthetic communities of diauxically shifting microbes.

Evidence for a multi-level trophic organization of the human gut microbiome

PLOS Computational Biology, 2019-12-19

Video Abstract (AI generated) Paper Preprint PLOS Computational Biology

The human gut microbiome is a complex ecosystem, in which hundreds of microbial species and metabolites coexist, in part due to an extensive network of cross-feeding interactions. However, both the large-scale trophic organization of this ecosystem, and its effects on the underlying metabolic flow, remain unexplored. Here, using a simplified model, we provide quantitative support for a multi-level trophic organization of the human gut microbiome, where microbes consume and secrete metabolites in multiple iterative steps. Using a manually-curated set of metabolic interactions between microbes, our model suggests about four trophic levels, each characterized by a high level-to-level metabolic transfer of byproducts. It also quantitatively predicts the typical metabolic environment of the gut (fecal metabolome) in approximate agreement with the real data. To understand the consequences of this trophic organization, we quantify the metabolic flow and biomass distribution, and explore patterns of microbial and metabolic diversity in different levels. The hierarchical trophic organization suggested by our model can help mechanistically establish causal links between the abundances of microbes and metabolites in the human gut.

Diversity, stability, and reproducibility in stochastically assembled microbial ecosystems

Physical Review Letters, 2018-04-13

Video Abstract (AI generated) Paper Preprint Physical Review Letters

Microbial ecosystems are remarkably diverse, stable, and often consist of a balanced mixture of core and peripheral species. Here we propose a conceptual model exhibiting all these emergent properties in quantitative agreement with real ecosystem data, specifically species' abundance and prevalence distributions. Resource competition and metabolic commensalism drive stochastic ecosystem assembly in our model. We demonstrate that even when supplied with just one resource, ecosystems can exhibit high diversity, increasing stability, and partial reproducibility between samples.