Microbial Potlatch: Cell-level adaptation of leakiness of metabolites leads to resilient symbiosis among diverse cells

Abstract

Microbial communities display extreme diversity, facilitated by the secretion of chemicals that can create new niches. However, it is unclear why cells often secrete even essential metabolites after evolution. By noting that cells can enhance their own growth rate by leakage of essential metabolites, we show that such leaker cells can benefit from coexistence with cells that consume the leaked chemicals in the environment. This leads to an unusual form of mutualism between "leaker" and "consumer" cells, resulting in frequency-dependent coexistence of multiple microbial species, as supported by extensive simulations. Remarkably, such symbiotic relationships generally evolve when each species adapts its leakiness to optimize its own growth rate under crowded conditions and nutrient limitations, leading to ecosystems with diverse species exchanging many metabolites with each other. In addition, such ecosystems are resilient against structural and environmental perturbations. Thus, we present a new basis for diverse, complex microbial ecosystems.