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The evolution of a novel trait can profoundly change an organism’s effects on its environment, which can in turn affect the further evolution of that organism and any coexisting organisms. We examine these effects and feedbacks following the evolution of a novel function in the Long-Term Evolution Experiment (LTEE) withEscherichia coli. A characteristic feature ofE. coliis its inability to grow aerobically on citrate (Cit⁻). Nonetheless, a Cit⁺variant with this capacity evolved in one LTEE population after 31 000 generations. The Cit⁺clade then coexisted stably with another clade that retained the ancestral Cit⁻phenotype. This coexistence was shaped by the evolution of a cross-feeding relationship based on C₄-dicarboxylic acids, particularly succinate, fumarate, and malate, that the Cit⁺variants release into the medium. Both the Cit⁻and Cit⁺cells evolved to grow on these excreted resources. The evolution of aerobic growth on citrate thus led to a transition from an ecosystem based on a single limiting resource, glucose, to one with at least five resources that were either shared or partitioned between the two coexisting clades. Our findings show that evolutionary novelties can change environmental conditions in ways that facilitate diversity by altering ecosystem structure and the evolutionary trajectories of coexisting lineages. 

Evolutionary innovations allow populations to colonize new ecological niches. We previously reported that aerobic growth on citrate (Cit+) evolved in an Escherichia coli population during adaptation to a minimal glucose medium containing citrate (DM25). Cit+ variants can also grow in citrate-only medium (DM0), a novel environment for E. coli. To study adaptation to this niche, we founded two sets of Cit+ populations and evolved them for 2500 generations in DM0 or DM25. The evolved lineages acquired numerous parallel mutations, many mediated by transposable elements. Several also evolved amplifications of regions containing the maeA gene. Unexpectedly, some evolved populations and clones show apparent declines in fitness. We also found evidence of substantial cell death in Cit+ clones. Our results thus demonstrate rapid trait refinement and adaptation to the new citrate niche, while also suggesting a recalcitrant mismatch between E. coli physiology and growth on citrate.