The Electron Transfer System of Syntrophically Grown Desulfovibrio vulgaris

Abstract

Interspecies hydrogen transfer between organisms producing and consuming hydrogen promotes the decomposition of organic matter in most anoxic environments. Although syntrophic coupling between hydrogen producers and consumers is a major feature of the carbon cycle, mechanisms for energy recovery at the extremely low free energies of reactions typical of these anaerobic communities have not been established. In this study, comparative transcriptional analysis of a model sulfate-reducing microbe, Desulfovibrio vulgaris Hildenborough, suggested the use of alternative electron transfer systems dependent on growth modality. During syntrophic growth on lactate with a hydrogenotrophic methanogen, numerous genes involved in electron transfer and energy generation were upregulated in D. vulgaris compared with their expression in sulfate-limited monocultures. In particular, genes coding for the putative membrane-bound Coo hydrogenase, two periplasmic hydrogenases (Hyd and Hyn), and the well-characterized high-molecular-weight cytochrome (Hmc) were among the most highly expressed and upregulated genes. Additionally, a predicted operon containing genes involved in lactate transport and oxidation exhibited upregulation, further suggesting an alternative pathway for electrons derived from lactate oxidation during syntrophic growth. Mutations in a subset of genes coding for Coo, Hmc, Hyd, and Hyn impaired or severely limited syntrophic growth but had little effect on growth via sulfate respiration. These results demonstrate that syntrophic growth and sulfate respiration use largely independent energy generation pathways and imply that to understand microbial processes that sustain nutrient cycling, lifestyles not captured in pure culture must be considered.Nutrient cycling on earth is determined primarily by cooperative interactions among microorganisms. The sharing of available energy within communities is particularly important in anaerobic systems, where limited energy is divided among highly specialized and metabolically interdependent populations (36,37,39). In the absence of exogenous electron acceptors such as sulfate and nitrate, the mineralization of organic matter in anoxic environments yields primarily carbon dioxide and methane, and this process is controlled by the synergistic activities of multiple anaerobic microbial populations. To better understand the metabolic basis and ecological significance of these syntrophic associations, we constructed an archetypical "community of two" by pairing Desulfovibrio vulgaris Hildenborough with a hydrogenotrophic methanogen, Methanococcus maripaludis strain S2.

Sustainable syntrophic growth of Dehalococcoides ethenogenes strain 195 with Desulfovibrio vulgaris Hildenborough and Methanobacterium congolense: global transcriptomic and proteomic analyses

“…This syntrophy occurs at trace sulfate concentrations. This approach of defined syntrophic growth enabled direct experimental measurement of the specific effects of associated bacteria on the growth, activity and gene expression of Dehalococcoides, similar to the approach taken for the study of Syntrophomonas wolfei with Methanospirillum hungatei (Beaty and McInerney, 1989), for the study of D. vulgaris with methanogens (Bryant et al, 1977;Scholten et al, 2007;Stolyar et al, 2007;Walker et al, 2009) and for the study of Desulfovibrio sp. strain SULF1 and Desulfovibrio fructosivorans with a dehalorespiring bacterium Desulfitobacterium frappieri TCE1 (Drzyzga et al, 2001;Drzyzga and Gottschal, 2002).…”

“…The down-regulation of these genes suggests that the syntrophic growth of DE195 and DVH might have a different hydrogen transfer system than the DE195 isolate. Transcriptomic analysis of DVH syntrophically grown with a hydrogenotrophic methanogen compared with DVH grown in sulfate-limited monocultures showed that genes encoding hydrogenases Coo, Hyd and Hyn were among the most highly expressed and up-regulated genes (Walker et al, 2009). Therefore, differential regulation of genes encoding hydrogenases of DVH grown in DE195/ DVH compared with the DVH isolate should be further investigated, to elucidate the interspecies hydrogen transfer during syntrophic growth.…”

Comparative analysis of metagenomes from three methanogenic hydrocarbon-degrading enrichment cultures with 41 environmental samples

“…The specific community structure may depend on the hydrocarbon substrates, the available nutrients and/or specific biogeochemical characteristics. Genes encoding anaerobic hydrocarbon-degrading enzymes (for example, bssA, assA) have been detected in hydrocarbon-degrading methanogenic cultures (for example Aitken et al, 2013;Cheng et al, 2013;Fowler et al, 2012;Washer and Edwards, 2007) as well as genes involved in syntrophic processes such as H 2 and formate transfer, and flagella, amino-acid and coenzyme biosynthesis (Kato et al, 2009;Walker et al, 2009). Despite recent reports of hydrocarbon-degrading co-cultures of sulfate reducers and methanogens (Callaghan et al, 2012;Lyles et al, 2014), the diversity of key enzymes and genes involved in methanogenic hydrocarbon metabolism are not yet well described.…”

Nutritional stress induces exchange of cell material and energetic coupling between bacterial species

“…Many studies have examined the syntrophic growth of sulfate-reducing bacteria (SRB) acting like secondary fermenters and methanogenic archaea [9][10][11] . Most recently, the metabolic interaction between Clostridia, acting as primary fermenters, and methanogenic archaea has also been studied 12,13 , highlighting a symbiotic process of interspecies hydrogen transfer that does not require physical interaction.…”