Microbial population dynamics decouple nutrient affinity from environmental concentration

Abstract

How the growth rate of a microbial population responds to the environmental availability of chemical nutrients and other resources is a fundamental question in microbiology. Models of this response, such as the widely-used Monod model, are generally characterized by a maximum growth rate and a half-saturation concentration of the resource. What values should we expect for these half-saturation concentrations, and how should they depend on the environmental concentration of the resource? We survey growth response data across a wide range of organisms and resources. We find that the half-saturation concentrations vary across orders of magnitude, even for the same organism and resource. To explain this variation, we develop an evolutionary model to show that demographic fluctuations (genetic drift) can constrain the adaptation of half-saturation concentrations. We find that this effect fundamentally differs depending on the type of population dynamics: populations undergoing periodic bottlenecks of fixed size will adapt their half-saturation concentration in proportion to the environmental resource concentration, but populations undergoing periodic dilutions of fixed size will evolve half-saturation concentrations that are largely decoupled from the environmental concentration. Our model not only provides testable predictions for laboratory evolution experiments, but it also reveals how an evolved half-saturation concentration may not reflect the organisms environment. In particular, this explains how organisms in resource-rich environments can still evolve fast growth at low resource concentrations. Altogether our results demonstrate the critical role of population dynamics in shaping fundamental ecological traits.