Emergent trade-offs among plasticity strategies in mixotrophs

Marine mixotrophs combine phagotrophy and phototrophy to acquire the resources they need for growth. Metabolic plasticity, the ability for individuals to dynamically alter their relative investment between different metabolic processes, allows mixotrophs to efficiently exploit variable environmental conditions. Different mixotrophs may vary in how quickly they respond to environmental stimuli, with slow-responding mixotrophs exhibiting a significant lag between a change in the environment and the resulting change metabolic strategy. In this study, we develop a model of mixotroph metabolic strategy and explore how the rate of the plastic response affects the seasonality, competitive fitness, and biogeochemical role of mixotroph populations. Fast-responding mixotrophs are characterized by more efficient resource use and higher average growth rates than slow-responding mixotrophs because any lag in the plastic response following a change in environmental conditions creates a mismatch between the mixotroph's metabolic requirements and their resource acquisition. However, this mismatch also results in increased storage of unused resources that support growth under future nutrient-limited conditions. As a result of this trade-off, mixotroph biomass and productivity are maximized at intermediate plastic response rates. Furthermore, the trade-off represents a mechanism for coexistence between fast-responding and slow-responding mixotrophs. In mixed communities, fast-responding mixotrophs are numerically dominant, but slow-responding mixotrophs persist at low abundance due to the provisioning effect that emerges as a result of their less efficient resource acquisition strategy. In addition to increased competitive ability, fast-responding mixotrophs are, on average, more autotrophic than slow-responding mixotrophs. Notably, these trade-offs associated with mixotroph response rate arise without including an explicit physiological cost associated with plasticity, a conclusion that may provide insight into evolutionary constraints of metabolic plasticity in mixotrophic organisms. When an explicit cost is added to the model, it alters the competitive relationships between fast- and slow-responding mixotrophs. Faster plastic response rates are favored by lower physiological costs as well as higher amplitude seasonal cycles.