Population dynamics of generalist/specialist strategies in the feast-famine cycle

Abstract

Microbial populations exhibit a broad spectrum of nutrient utilization strategies, ranging from those utilizing diverse nutrients, called "generalists," to those being highly adapted to specific nutrients, called "specialists." Identifying the conditions for the diversification of nutrient utilization strategies is one of the central questions in ecology. Previous theoretical studies have shown that trade-offs among different resource utilization functions in which cells cannot utilize broad types of substrates at nearly optimal efficiency are crucial for the emergence of diverse strategies. Additionally, in natural settings, nutrient availability often fluctuates over time, imposing another trade-off on the cells. Cells that grow rapidly under nutrient-rich conditions tend to have a higher death rate under nutrient-poor conditions, leading to a growth-death trade-off. This additional trade-off can contribute to the emergence of diverse strategies. Here, we introduce a mathematical model that simultaneously incorporates the resource-use trade-off and the growth-death trade-off. Nutrient supply was modeled as discrete stochastic events, mimicking temporal changes in nutrient availability. We show that the phenotype with a higher ratio of growth rate to death rate dominates the population; that is, the strength of the growth-death trade-off is a major determinant of whether generalists or specialists are dominant. We also found that a sparse and uncertain nutrient supply favors specialists, increasing their temporally averaged abundance. Our findings reveal that accounting for temporal environmental variation and the resulting growth-death trade-off is crucial for understanding the drivers of diversification in microbial nutrient utilization strategies. Author summaryMicrobial strategies for choosing the nutrients to utilize are highly diverse. In our study, we explored why some microbes become generalists able to use a variety of nutrients, whereas others specialize in only a few nutrients. These strategies often result from metabolic trade-offs during nutrient processing. However, in fluctuating environmental conditions, it is important to consider additional trade-offs; under nutrient-rich conditions, they can grow quickly, but this often comes at the cost of being more vulnerable when nutrients are scarce. To investigate how these trade-offs affect the emergence of generalists and specialists, we developed a simple model called the feast-famine cycle that mimics the natural cycles of plenty and scarcity of nutrients. Our work shows that the trade-off between growth and death rates is crucial for determining whether a generalist or specialist strategy is dominant. We highlight the importance of trade-offs in response to environmental changes in shaping microbial adaptive strategies.