Adaptation of metabolite leakiness leads to symbiotic chemical exchange and to a resilient microbial ecosystem

Abstract

Microbial communities display remarkable 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. Based on theoretical results indicating that cells can enhance their own growth rate by leaking even essential metabolites, we show that such “leaker” cells can establish an asymmetric form of mutualism with “consumer” cells that consume the leaked chemicals: the consumer cells benefit from the uptake of the secreted metabolites, while the leaker cells also benefit from such consumption, as it reduces the metabolite accumulation in the environment and thereby enables further secretion, resulting in frequency-dependent coexistence of multiple microbial species. As supported by extensive simulations, such symbiotic relationships generally evolve when each species has a complex reaction network and adapts its leakiness to optimize its own growth rate under crowded conditions and nutrient limitations. Accordingly, symbiotic ecosystems with diverse cell species that leak and exchange many metabolites with each other are shaped by cell-level adaptation of leakiness of metabolites. Moreover, the resultant ecosystems with entangled metabolite exchange are resilient against structural and environmental perturbations. Thus, we present a theory for the origin of resilient ecosystems with diverse microbes mediated by secretion and exchange of essential chemicals.

The role of competition versus cooperation in microbial community coalescence

“…Leakage of metabolic resources is a pervasive phenomenon in the microbial world [38, 39], and has been shown to exist also in resources necessary for growth, even in situations when those essential metabolites are scarce [40, 41]. Although it may seem counter-intuitive for microbes to secrete metabolites essential for their own growth, such leakage can be advantageous, especially in bacteria, as “flux control” or growth-dilution mechanisms which provide short-term growth benefits in crowded environments [42, 43].…”

Metabolism Interactions Promote the Overall Functioning of the Episymbiotic Chemosynthetic Community of Shinkaia crosnieri of Cold Seeps

“…Microbe-microbe interactions, including cooperative, competitive, and predatory interactions have been suggested as critical for ensuring community specificity, particularly in open systems ( 23 , 24 ). Among these interaction types, cooperation plays a particularly significant role in maintaining complex community structures ( 25 ), improving stress resistance ( 26 ), and increasing community productivity ( 27 ). The Black Queen Hypothesis states that bacterial populations unavoidably leak public goods (e.g., nutrients or metabolites) that are then available to the entire community and could lead to metabolite dependencies and adaptive gene loss and promote the coexistence of diverse bacterial taxa ( 25 , 28 ).…”

“…For example, dependency has been suggested to increase the coexistence of species via waste-product exploitation ( 29 ). Furthermore, these interdependent cooperative interactions provide considerable selective advantages to bacterial species ( 26 , 30 , 31 ). In episymbiotic communities, dominant chemosynthetic bacteria are primary producers and are more likely to exude public goods, thereby promoting metabolic interactions.…”

Stability criteria for the consumption and exchange of essential resources

“…Consumers in our model also leak some byproducts from the processes that convert resources to biomass. We interpret this leakage as an inefficiency due to the permeability of cell membranes, but there may also be evolutionary reasons why microbes secrete metabolites [ 30 ]. We assume that constant fractions, θ , of the resources used to build biomass are transformed into byproducts, as described by another matrix , which can be different from P .…”