Stability of multi-species consortia during microbial metabolic evolution

Explaining multi-genic adaptations is a major objective of evolutionary theory. Metabolic pathways require multiple functional enzymes to generate a phenotype, and their evolution in microbes remains underexplored. In particular, sites polluted with manmade chemicals or "xenobiotics", like plastic or pesticides, provide evidence for the rapid adaptation of novel metabolic pathways in microbes, which degrade these xenobiotics into utilizable nutrients. Decades of microbiological studies revealed that these pathways often are not consolidated within a single microbial species but are rather distributed across several different species cooperatively degrading xenobiotics. These diverse consortia are remarkably stable in the laboratory, but the determinants of this stability have not been hereto addressed. In this study, we predict barriers to stable co-existence arising from the metabolic roles each species plays in the novel metabolic pathway. Then, we show that ecological variation in microbial life history overcomes these barriers and explains stable co-existence in mathematical models of exemplary consortia growing on a xenobiotic as the sole source of a limiting nutrient. Stability hinges on an "ecological matching" between a species' metabolic role and its nutrient utilization strategy, which, if satisfied, can greatly accelerate the evolution of metabolic pathways in both field and laboratory.