Comprehensive Bioenergetic Evaluation of Microbial Pathway Variants in Syntrophic Propionate Oxidation

In this work, an original methodology was developed that quantifies bioenergetically and physiologically feasible net ATP yields for large numbers of microbial metabolic pathways and their variants under different conditions. All variants are evaluated, which ensures global optimality in finding the pathway variant(s) leading to the highest ATP yield. The methodology is designed to be especially relevant to hypothesize on which microbial pathway variants should be most favored in microbial ecosystems under high selective pressure for efficient metabolic energy conservation. Syntrophic microbial oxidation of propionate to acetate has an extremely small quantity of available energy and requires an extremely high metabolic efficiency to sustain life. Our results bring mechanistic insights into the optimum pathway variants, other metabolic bottlenecks, and the impact of environmental conditions on the ATP yields. Additionally, our results conclude that, as previously reported, under specific conditions, IET mechanisms other than hydrogen must exist to simultaneously sustain the growth of both propionate oxidizers and hydrogenotrophic methanogens.