Minorities drive growth resumption in cross-feeding microbial communities

Abstract

Microbial communities are fundamental to life on Earth. Different strains within these communities are often connected by a highly connected metabolic network, where the growth of one strain depends on the metabolic activities of other community members. While distributed metabolic functions allow microbes to reduce costs and optimize metabolic pathways, they make them metabolically dependent. Here, we hypothesize that such dependencies can be detrimental in situations where the external conditions change rapidly, as they often do in natural environments. After a shift in external conditions, microbes need to remodel their metabolism, but they can only resume growth once partners on which they depend have also adapted to the new conditions. It is currently not well understood how microbial communities resolve this dilemma and how metabolic interactions are reestablished after an environmental shift. To address this question, we investigated the dynamical responses to environmental perturbation by microbial consortia with distributed anabolic functions. By measuring the regrowth times at the single-cell level in spatially structured communities, we found that metabolic dependencies lead to a growth delay after an environmental shift. However, a minority of cells—those in the immediate neighborhood of their metabolic partners—can regrow quickly and come to numerically dominate the community after the shift. The spatial arrangement of a microbial community is thus a key factor in determining the communities’ ability to maintain metabolic interactions and growth in fluctuating conditions. Our results suggest that environmental fluctuations can limit the emergence of metabolic dependencies between microorganisms.