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Metabolic cross-feeding plays vital roles in promoting ecological diversity. While some microbes depend on exchanges of essential nutrients for growth, the forces driving the extensive cross-feeding needed to support the coexistence of free-living microbes are poorly understood. Here we characterize bacterial physiology under self-acidification and establish that extensive excretion of key metabolites following growth arrest provides a collaborative, inter-species mechanism of stress resistance. This collaboration occurs not only between species isolated from the same community, but also between unrelated species with complementary (glycolytic vs. gluconeogenic) modes of metabolism. Cultures of such communities progress through distinct phases of growth-dilution cycles, comprising of exponential growth, acidification-triggered growth arrest, collaborative deacidification, and growth recovery, with each phase involving different combinations of physiological states of individual species. Our findings challenge the steady-state view of ecosystems commonly portrayed in ecological models, offering an alternative dynamical view based on growth advantages of complementary species in different phases.

 

The ubiquitous existence of microbial communities marks the importance of understanding how species interact within the community to coexist and their spatial organization. We study a two-species mutualistic cross-feeding model through a stochastic cellular automaton on a square lattice using kinetic Monte Carlo simulation. Our model encapsulates the essential dynamic processes such as cell growth, and nutrient excretion, diffusion and uptake. Focusing on the interplay among nutrient diffusion and individual cell division, we discover three general classes of colony morphology: co-existing sectors, co-existing spirals, and engulfment. When the cross-feeding nutrient is widely available, either through high excretion or fast diffusion, a stable circular colony with alternating species sector emerges. When the consumer cells rely on being spatially close to the producers, we observe a stable spiral. We also see one species being engulfed by the other when species interfaces merge due to stochastic fluctuation. By tuning the diffusion rate and the growth rate, we are able to gain quantitative insights into the structures of the sectors and the spirals.