Paradoxes in Leaky Microbial Trade

Abstract

Microbes produce metabolic resources that are important for cell growth yet leak across membranes into the extracellular environment. Other microbes in the same environment can use these resources and adjust their own metabolic production accordingly--causing other resources to leak into the environment. The combined effect of these processes is an economy in which organismal growth and metabolic production are coupled to others in the community. We propose a model for the co-evolving dynamics of metabolite concentrations, production regulation, and population frequencies for the case of two cell types, each requiring and capable of producing two metabolites. In this model, beneficial trade relations emerge without any coordination, via individual-level production decisions that maximize each cells growth rate given its perceived environment. As we vary production parameters of the model, we encounter three paradoxical behaviors, where a change that should intuitively benefit some cell type, actually harms it. (1) If a cell type is more efficient than its counterpart at producing a metabolite and becomes even more efficient, its frequency in the population can decrease. (2) If a cell type is less efficient than its counterpart at producing a metabolite but becomes less inefficient, the growth rate of the population can decrease. (3) Finally, if a cell type controls its counterparts production decisions so as to maximize its own growth rate, the ultimate growth rate it achieves can be lower than if the two cell types each maximized their own growth. These three paradoxes highlight the complex and counter-intuitive dynamics that emerge in simple microbial economies.