Emergent ecological advantage of sequential metabolic strategies in complex microbial communities

Microbes adopt a variety of metabolic strategies to consume resources in fluctuating environments. Most work has focused on understanding these strategies physiologically for the growth of single species, rather than ecologically for the assembly of complex natural communities. Here, using a new consumer-resource framework incorporating dynamic proteome re-allocation, we compare the two dominant metabolic strategies among microbes: sequential (diauxie) and co-utilization of resources. We find that even when sequential strategies are worse in pairwise competitions, they can clearly dominate in complex multi-species communities. This emergent ecological advantage of sequential strategies lies in their growth rate distributions, specifically their wider upper tails despite lower average growth rates. While average growth rates are important when the level of competition is low, the tails matter in mature communities where the level of competition is high. We also find that both strategies stratify by species richness of communities, with sequential strategies dominating species-rich communities and co-utilizers dominating low-diversity communities with only 1–2 species. Sequential species can more efficiently pack resource niches due to their increased resilience to environmental fluctuations in resource ratios, i.e., their structural stability. Overall, our work provides an explanation for the long-standing puzzle of how sequential and co-utilizing strategies coexist in nature, and provides several testable predictions about their co-occurrence patterns.