Heterotrophic substrate specificity in the aquatic environment: The role of microscale patchiness investigated using modelling

Recent observations of natural bacterial communities show high genetic diversity in organic carbon uptake systems (microdiversity) and specificity in substrate species taken up. This seemingly contradicts a large body of literature from laboratory experiments under nutrient-limiting conditions, where mixed substrate use is the rule. This apparent discrepancy can be resolved by realizing that bacteria in the natural aquatic environment encounter nutrients as high-concentration patches. They may live in an ecologically nutrient-limiting environment, but they are rarely in a biologically nutrient-limited state. Rather they switch between non-growing and nutrient-replete states. During nutrient-replete growth the metabolism is saturated and assimilating additional substrates does not increase the growth rate, but carrying the assimilation system constitutes a cost. Consequently, the specialist strategy is beneficial, which is consistent with observations from laboratory experiments. When the bacteria are not growing, the added cost also reduces the fitness of the generalist species. A simple mathematical model encompassing the relevant mechanisms is developed and parameterized realistically based on the literature. The model predicts that, under pulsed conditions, specialization is beneficial when the metabolic cost of an additional uptake system is more than similar to 0.5% of the total metabolic cost, which is a reasonable estimate and illustrates that this is a plausible hypothesis.