Synergistic epistasis enhances cooperativity of mutualistic interspecies interactions

Abstract

SUMMARYFrequent fluctuations in sulfate availability rendered syntrophic interactions between the sulfate reducing bacterium Desulfovibrio vulgaris (Dv) and the methanogenic archaeon Methanococcus maripaludis (Mm) unsustainable. By contrast, prolonged laboratory evolution in obligate syntrophy conditions improved the productivity of this community but at the expense of erosion of sulfate respiration (SR). Hence, we sought to understand the evolutionary trajectories that could both increase the productivity of syntrophic interactions and sustain SR. We combined a temporal and combinatorial survey of mutations accumulated over 1000 generations of 9 independently-evolved communities with analysis of the genotypic structure for one community down to the single-cell level. We discovered a high level of parallelism across communities despite considerable variance in their evolutionary trajectories and the perseverance of a rare SR+ Dv lineage within many evolution lines. An in-depth investigation revealed that synergistic epistasis across Dv and Mm genotypes had enhanced cooperativity within SR- and SR+ assemblages, allowing their co-existence as r- and K-strategists, respectively.

Novel Mode of Molybdate Inhibition of Desulfovibrio vulgaris Hildenborough

“…It is possible that, rather than acting directly on molybdate, another product of DVU2210 is causing molybdate sensitivity and, thus, the deletion provides some resistance. Mutations have been described to occur within DVU2210 in evolved cocultures of D. vulgaris Hildenborough and Methanococcus maripaludis in which interspecies electron transfer occurs in the absence of sulfate ( Turkarslan et al, 2020 ). Interestingly, mutations in sat of D. vulgaris Hildenborough have also been described during evolution of these organisms in coculture and resulted in a loss of sulfate-reduction capacity of the D. vulgaris ( Hillesland et al, 2014 ).…”

“…To our knowledge, the coculture has not been tested for resistance to molybdate. Recent genome analysis of isolates from these evolved cocultures suggests that the mutations in sat and DVU2210 are mutually exclusive; both mutations are present in the community, but apparently not within the same cells ( Turkarslan et al, 2020 ). Thus, we would predict that molybdate would still be inhibitory in the culture.…”

“…The D. vulgaris and methanogen coculture evolution described previously ( Turkarslan et al, 2020 ) and the Δ sat adaptation to molybdate in this study were both performed in the absence of sulfate and resulted in selection of mutations of DVU2210. We do not know if the absence of sulfate altered the selective pressure.…”