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In microbial systems, a metabolic pathway can be either completed by one autonomous population or distributed among a consortium performing metabolic division of labor (MDOL). MDOL facilitates the system's function by reducing the metabolic burden; however, it may hinder the function by reducing the exchange efficiency of metabolic intermediates among individuals. As a result, the function of a community is influenced by the trade-offs between the metabolic specialization and versatility of individuals. To experimentally test this hypothesis, we deconstructed the naphthalene degradation pathway into four steps and introduced them individually or combinatorically into different strains with varying levels of metabolic specialization. Using these strains, we engineered 1,456 synthetic consortia and found that 74 consortia exhibited higher degradation function than both the autonomous population and rigorous MDOL consortium. Quantitative modeling provides general strategies for identifying the most effective MDOL configuration. Our study provides critical insights into the engineering of high-performance microbial systems.

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In fluctuating nutrient environments, isogenic microbial cells transition into "multicellular" communities composed of phenotypically heterogeneous cells, showing functional specialization. In fungi (such as budding yeast), phenotypic heterogeneity is often described in the context of cells switching between different morphotypes (e.g., yeast to hyphae/pseudohyphae or white/opaque transitions in Candida albicans). However, more fundamental forms of metabolic heterogeneity are seen in clonal Saccharomyces cerevisiae communities growing in nutrient-limited conditions. Cells within such communities exhibit contrasting, specialized metabolic states, and are arranged in distinct, spatially organized groups. In this study, we explain how such an organization can stem from self-organizing biochemical reactions that depend on special metabolites. These metabolites exhibit plasticity in function, wherein the same metabolites are metabolized and utilized for distinct purposes by different cells. This in turn allows cell groups to function as specialized, interdependent cross-feeding systems which support distinct metabolic processes. Exemplifying a system where cells exhibit either gluconeogenic or glycolytic states, we highlight how available metabolites can drive favored biochemical pathways to produce new, limiting resources. These new resources can themselves be consumed or utilized distinctly by cells in different metabolic states. This thereby enables cell groups to sustain contrasting, even apparently impossible metabolic states with stable transcriptional and metabolic signatures for a given environment, and divide labor in order to increase community fitness or survival. We speculate on possible evolutionary implications of such metabolic specialization and division of labor in isogenic microbial communities.

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BACKGROUND: Human-to-human transmission of symbiotic, anaerobic bacteria is a fundamental evolutionary adaptation essential for membership of the human gut microbiota. However, despite its importance, the genomic and biological adaptations underpinning symbiont transmission remain poorly understood. The Firmicutes are a dominant phylum within the intestinal microbiota that are capable of producing resistant endospores that maintain viability within the environment and germinate within the intestine to facilitate transmission. However, the impact of host transmission on the evolutionary and adaptive processes within the intestinal microbiota remains unknown. RESULTS: We analyze 1358 genomes of Firmicutes bacteria derived from host and environment-associated habitats. Characterization of genomes as spore-forming based on the presence of sporulation-predictive genes reveals multiple losses of sporulation in many distinct lineages. Loss of sporulation in gut Firmicutes is associated with features of host-adaptation such as genome reduction and specialized metabolic capabilities. Consistent with these data, analysis of 9966 gut metagenomes from adults around the world demonstrates that bacteria now incapable of sporulation are more abundant within individuals but less prevalent in the human population compared to spore-forming bacteria. CONCLUSIONS: Our results suggest host adaptation in gut Firmicutes is an evolutionary trade-off between transmission range and colonization abundance. We reveal host transmission as an underappreciated process that shapes the evolution, assembly, and functions of gut Firmicutes.

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All biosynthetically active cells are able to export and import metabolites, the small molecule intermediaries of metabolism. In dense cell populations, this hallmark of cells results in the intercellular exchange of a wide spectrum of metabolites. Such metabolite exchange enables metabolic specialization of individual cells, leading to far reaching biological implications, as a consequence of the intrinsic connection between metabolism and cell physiology. In this chapter, we discuss methods on how to study metabolite exchange interactions by using self-establishing metabolically cooperating communities (SeMeCos) in the budding yeast Saccharomyces cerevisiae. SeMeCos exploit the stochastic segregation of episomes to progressively increase the number of essential metabolic interdependencies in a community that grows out from an initially prototrophic cell. By coupling genotype to metabotype, SeMeCos allow for the tracking of cells while they specialize metabolically and hence the opportunity to study their progressive change in physiology.

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While most Vibrionaceae are considered generalists that thrive on diverse substrates, including animal-derived material, we show that Vibrio breoganii has specialized for the consumption of marine macroalga-derived substrates. Genomic and physiological comparisons of V. breoganii with other Vibrionaceae isolates revealed the ability to degrade alginate, laminarin, and additional glycans present in algal cell walls. Moreover, the widely conserved ability to hydrolyze animal-derived polymers, including chitin and glycogen, was lost, along with the ability to efficiently grow on a variety of amino acids. Ecological data showing associations with particulate algal material but not zooplankton further support this shift in niche preference, and the loss of motility appears to reflect a sessile macroalga-associated lifestyle. Together, these findings indicate that algal polysaccharides have become a major source of carbon and energy in V. breoganii, and these ecophysiological adaptations may facilitate transient commensal associations with marine invertebrates that feed on algae.IMPORTANCE Vibrios are often considered animal specialists or generalists. Here, we show that Vibrio breoganii has undergone massive genomic changes to become specialized on algal carbohydrates. Accompanying genomic changes include massive gene import and loss. These vibrios may help us better understand how algal biomass is degraded in the environment and may serve as a blueprint on how to optimize the conversion of algae to biofuels.

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Adaptation to any given environment may be accompanied by a cost in terms of reduced growth in the ancestral or some alternative environment. Ecologists explain the cost of adaptation through the concept of a trade-off, by which gaining a new trait involves losing another trait. Two mechanisms have been invoked to explain the evolution of trade-offs in ecological systems, mutational degradation, and functional interference. Mutational degradation occurs when a gene coding a specific trait is not under selection in the resident environment; therefore, it may be degraded through the accumulation of mutations that are neutral in the resident environment but deleterious in an alternative environment. Functional interference evolves if the gene or a set of genes have antagonistic effects in two or more ecologically different traits. Both mechanisms pertain to a situation where the selection and the alternative environments are ecologically different. To test this hypothesis, we conducted an experiment in which 12 experimental populations of wild yeast were each grown in a minimal medium supplemented with a single substrate. We chose 12 different carbon substrates that were metabolized through similar and different pathways in order to represent a wide range of ecological conditions. We found no evidence for trade-offs between substrates on the same pathway. The indirect response of substrates on other pathways, however, was consistently negative, with little correlation between the direct and indirect responses. We conclude that the grain of specialization in this case is the metabolic pathway and that specialization appears to evolve through mutational degradation.