Fitness advantage of sequential metabolic strategies emerges from community interactions in strongly fluctuating environments

Microbes growing in fluctuating environments employ two key metabolic strategies: sequential (diauxic) utilization and co-utilization of nutrients. Most work has focused on understanding and comparing these strategies physiologically for the growth of single species, rather than ecologically for the assembly of complex natural communities. This is in part because of the lack of a framework for directly comparing the fitness of these strategies in an ecological context. Here, we present a new consumer-resource framework that incorporates dynamic proteome reallocation, and use it to compare the fitness of metabolic strategies during community assembly. We introduce two notions of fitness of a strategy in fluctuating environments: the time-averaged growth rate and the biomass-weighted prevalence of microbes using a given strategy. We find that sequential utilizers, although disadvantaged in pairwise competitions, gain a significant edge during community assembly - an advantage that becomes more pronounced with increasing community diversity and the size of the species pool from which they are assembled. Low diversity communities resemble pairwise competitions and are dominated by co-utilizers, whereas high diversity, mature communities (i.e., those assembled from a larger species pool) are dominated by the sequential utilizers. This shift is driven by two factors: the difference in lag times and the increased structural stability conferred by sequential strategies. Overall, our work provides several testable predictions about the co-occurrence patterns of microbes using different metabolic strategies.