A stable genetic polymorphism underpins microbial syntrophy in an anaerobic reactor

Syntrophies are metabolic cooperations, whereby two organisms co-metabolize a substrate in an interdependent manner. They are common in natural microbial communities and constitute a desired motifs in engineered synthetic microbial communities. Many of the observed natural syntrophic interactions are mandatory in the absence of strong electron acceptors, such that one species in the syntrophy has to assume the role of electron sink for the other. This generates the problem for the involved species of how to split the available energy of the total metabolic reaction between them. Here, we show that the syntrophic sulfate reducing species Desulfovibrio vulgaris displays a stable genetic polymorphism, where two distinct genotypes differ in their ability to engage in syntrophy with the hydrogenotrophic methanogen Methanococcus maripaludis. These two genotypes differ by two genetic alterations, one of which is associated with a single amino acid deletion in the proton translocating subunit cooK of the membrane-bound COO-hydrogenase. We show that this latter alteration leads to reshaping of energy conservation in the lactate oxidation pathway of D.vulgaris, thereby enabling sufficient intermediate metabolite production for sustaining M. maripaludis growth. These findings provide a detailed understanding on the genetic basis of syntrophy in nature and bring us closer to rational engineering of syntrophy in synthetic communities.