Timescale of environmental change modulates metabolic guild cohesion in microbial communities

Abstract Microbial communities experience environmental fluctuations across timescales from rapid changes in moisture, temperature, or light levels to long-term seasonal or climactic variations. Understanding how microbial populations respond to these changes is critical for predicting the impact of perturbations, interventions, and climate change on communities. Because communities typically harbor tens to hundreds of distinct taxa, the response of microbial abundances to perturbations is potentially complex. However, even though taxonomic diversity is high, in many communities taxa can be grouped into metabolic guilds of strains with similar metabolic traits. These guilds effectively reduce the complexity of the system by providing a physiologically motivated coarse-graining. Here, using a combination of simulations, theory, and experiments, we show that the response of guilds to nutrient fluctuations depends on the timescale of those fluctuations. Rapid changes in nutrient levels drive cohesive, positively correlated abundance dynamics within guilds. For slower timescales of environmental variation, members within a guild begin to compete due to similar resource preferences, driving negative correlations in abundances between members of the same guild. Our results provide a route to understanding the relationship between metabolic guilds and community response to changing environments, as well as an experimental approach to discovering metabolic guilds via designed nutrient perturbations to communities.