Model selection for microbial nutrient uptake using a cost-benefit approach

•The control of bacterial substrate utilization is modeled by optimization principles.•We use parsimonious model structures tailored to biochemical pathway topologies.•Depending on the pathway topology, we identify three prototypical uptake pattern.•We find (1) parallel consumption, (2) catabolite repression, and (3) bistable uptake.•We use this model to analyze experiments with Geobacter metallireducens. We consider the uptake of various carbon sources by microorganisms based on four fundamental assumptions: (1) the uptake of nutrient follows a saturation characteristics (2) substrate processing has a benefit but comes at costs of maintaining the process chain (3) substrate uptake is controlled and (4) evolution optimized the control of substrate uptake. These assumptions result in relatively simple mathematical models. In case of two substrates, our main finding is the following: Depending on the overall topology of the metabolic pathway, three different behavioral patterns can be identified. (1) both substrates are consumed at a time, (2) one substrate is preferred and represses the uptake of the other (catabolite repression), or (3) a cell feeds exclusively on one or the other substrate, possibly leading to a population that splits in two sub-populations, each of them specialized on one substrate only. Batch-culture and retentostat data of toluene, benzoate, and acetate uptake by Geobacter metallireducens are used to demonstrate that the model structure is suited for a quantitative description of uptake dynamics.