Proteome allocation and the evolution of metabolic cross-feeding

Abstract

AbstractMetabolic cross-feeding (MCF) is a widespread type of ecological interaction where organisms share nutrients. In a common instance of MCF, an organism incompletely metabolizes sugars and releases metabolites that are used by another as a carbon source to produce energy. Why would the former waste edible food, and why does this preferentially occur at specific locations in the sugar metabolic pathway (acetate and glycerol are preferentially exchanged) have challenged evolutionary theory for decades. After showing that cells should in principle prioritise upstream reactions, we investigate how a special feature of these metabolites – their high diffusivity across the cell membrane – may trigger the emergence of cross feeding in a population. We explicitly model metabolic reactions, their enzyme-driven catalysis, and the cellular constraints on the proteome that may incur a cost to expressing all enzymes along the metabolic pathway. We find that up to high permeability coefficients of an intermediate metabolite, the expected evolutionary outcome is not a diversification that resembles cross-feeding but a single genotype that instead overexpresses the enzymes downstream the metabolite to limit its diffusion. Only at very high permeabilities and under restricted sets of parameters should the population diversify and MCF evolve.