Microbial population dynamics decouple growth response from environmental nutrient concentration

Abstract

How the growth rate of a microbial population depends on the availability of chemical nutrients and other resources in the environment is a fundamental question in microbiology. Models of this dependence, such as the well-known Monod model, are characterized by a threshold concentration (or affinity) of the resource, above which the population can grow near its maximum rate. Even though this concept is a core element of microbiological and ecological modeling, there is little empirical and theoretical evidence for the evolved diversity of these thresholds. In particular, does resource scarcity drive populations to evolve commensurately lower thresholds? To address this question, we perform the largest-to-date meta-analysis of resource threshold data across a wide range of organisms and resources, substantially expanding previous surveys. We find that the thresholds 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 resource thresholds. We find that this effect fundamentally differs depending on the type of population dynamics: populations undergoing periodic bottlenecks of fixed size will adapt their thresholds in proportion to the environmental resource concentration, but populations undergoing periodic dilutions of fixed size will evolve thresholds 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 resource threshold may not reflect the organism's environment. In particular, this explains how organisms in nutrient-rich environments can still evolve facultative growth at low resource concentrations. Altogether our results demonstrate the critical role of population dynamics in shaping fundamental ecological traits.

Dynamic coexistence driven by physiological transitions in microbial communities

“…Their work has often been dismissed (including in their own paper [47]) as a mathematical observation relevant only for an assumed growthaffinity trade-off, narrow resource competition, and other idealizations. Our work argues that their simple mechanism of dynamic coexistence -also explored in recent works [41,[48][49][50][51][52] -is more relevant, not less, given the observed complex physiology and nonlinear growth dependencies in real microbial ecosystems. If physiological state changes turn out to be dominant drivers of dynamical niches, as seen in [12,16,53], dynamics cannot be "averaged" over but become the essential link between physiology and ecology.…”

Bacterial BEF relationships: degradation metabolic trade-offs with growth rate but not with nitrogen processing pathways

“…Evidently, the necessity for insect-derived nitrogen is not a considerable driver behind bacterial nitrogen processing. While cultures were not grown within the host plant for the duration of the experiment, and therefore were not directly in uenced by the nutrient requirements of the host, microbial growth rates correlate more with the nutrient availability they evolved with than the current nutrient availability [44]. Despite these expectations, ammonia and nitrate concentration had no correlation with degradative function, indicating that insect degradation is not driven solely by nitrogen requirements of the plant.…”