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.

The role of competition versus cooperation in microbial community coalescence

“…Ultimately, competition in the for leaked resources exists because bacteria are secreting resources necessary for their own growth. While this might seem disadvantageous, and thus unrealistic at first, leaking essential metabolites is an observed phenomenon in many microbial systems [35,36], and may be advantageous as a "flux control" mechanism employed by individual cells to promote growth in crowded environments [37,38]. Overall, this finding extends the results of previous theoretical studies to accommodate metabolic interdependence; an essential feature of microbial communities, thus constituting a more robust result supporting experimental findings [25] and hypotheses [39].…”

“…Ultimately, competition in the biotically-generated resource space exists because bacteria are leaking resources necessary for their own growth. While this might seem disadvantageous, and thus unrealistic at first, leaking essential metabolites is an observed phenomenon in many microbial systems [35,36], and may be advantageous as a "flux control" mechanism employed by individual cells to promote growth in crowded environments [37,38].…”