bThe mineralization of organic matter in anoxic environments relies on the cooperative activities of hydrogen producers and consumers obligately linked by interspecies metabolite exchange in syntrophic consortia that may include sulfate reducing species such as Desulfovibrio. To evaluate the metabolic flexibility of syntrophic Desulfovibrio to adapt to naturally fluctuating methanogenic environments, we studied Desulfovibrio alaskensis strain G20 grown in chemostats under respiratory and syntrophic conditions with alternative methanogenic partners, Methanococcus maripaludis and Methanospirillum hungatei, at different growth rates. Comparative whole-genome transcriptional analyses, complemented by G20 mutant strain growth experiments and physiological data, revealed a significant influence of both energy source availability (as controlled by dilution rate) and methanogen on the electron transfer systems, ratios of interspecies electron carriers, energy generating systems, and interspecies physical associations. A total of 68 genes were commonly differentially expressed under syntrophic versus respiratory lifestyle. Under low-energy (low-growth-rate) conditions, strain G20 further had the capacity to adapt to the metabolism of its methanogenic partners, as shown by its differing gene expression of enzymes involved in the direct metabolic interactions (e.g., periplasmic hydrogenases) and the ratio shift in electron carriers used for interspecies metabolite exchange (hydrogen/formate). A putative monomeric [Fe-Fe] hydrogenase and Hmc (high-molecular-weight-cytochrome c 3 ) complex-linked reverse menaquinone (MQ) redox loop become increasingly important for the reoxidation of the lactate-/pyruvate oxidation-derived redox pair, DsrC red and Fd red , relative to the Qmo-MQ-Qrc (quinone-interacting membrane-bound oxidoreductase; quinone-reducing complex) loop. Together, these data underscore the high enzymatic and metabolic adaptive flexibility that likely sustains Desulfovibrio in naturally fluctuating methanogenic environments.
In anoxic environments depleted in inorganic electron acceptors (e.g., freshwater and marine sediments, flooded soils, landfills and sewage digestors) the complete mineralization of complex organic matter to CO 2 and methane relies on the cooperative activities of phylogenetically and metabolically distinct microbial groups assembled in syntrophic consortia (1-3). In these assemblages, sulfate-reducing bacteria (SRB) such as Desulfovibrio species function as secondary fermenters obligately linked via interspecies electron transfer to the metabolic activity of methanogenic archaea, since the oxidation of common substrates (organic acids and alcohols) only yields sufficient energy for cell maintenance and growth when the methanogens maintain low concentrations of the SRB metabolites (1-3). Hydrogen and formate are considered to be the primary shuttle compounds for interspecies electron transfer in methanogenic consortia (1-3). Exclusive use of H 2 as an electron carrier has been proven for severa...