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A detailed understanding of gut microbial ecology is essential to engineer effective microbial therapeutics and to model microbial community assembly and succession in health and disease. However, establishing generalizable insights into the functional determinants of microbial fitness in the human gut has been a formidable challenge. Here we employ fecal microbiota transplantation (FMT) as an in natura experimental model to identify determinants of microbial colonization and resilience. Our long-term sampling strategy and high-resolution multi-omics analyses of FMT donors and recipients reveal adaptive ecological processes as the main driver of microbial colonization outcomes after FMT. We also show that high-fitness donor microbial populations are significantly enriched in metabolic pathways that are responsible for the biosynthesis of nucleotides, essential amino acids, and micronutrients, independent of taxonomy. To determine whether such metabolic competence can explain the microbial ecology of human disease states, we analyzed genomes reconstructed from healthy humans and humans with inflammatory bowel disease (IBD). Our data reveal that such traits are also significantly enriched in microbial genomes recovered from IBD patients, linking presence of superior metabolic competence in bacteria to their expansion in IBD. Overall, these findings suggest that the transfer of gut microbes from a healthy donor to a disrupted recipient environment initiates an environmental filter that selects for populations that can self- sustain. Such ecological processes that select for self-sustenance under stress offer a model to explain why …