Variation among Desulfovibrio Species in Electron Transfer Systems Used for Syntrophic Growth

Abstract

bMineralization of organic matter in anoxic environments relies on the cooperative activities of hydrogen producers and consumers linked by interspecies electron transfer in syntrophic consortia that may include sulfate-reducing species (e.g., Desulfovibrio). Physiological differences and various gene repertoires implicated in syntrophic metabolism among Desulfovibrio species suggest considerable variation in the biochemical basis of syntrophy. In this study, comparative transcriptional and mutant analyses of Desulfovibrio alaskensis strain G20 and Desulfovibrio vulgaris strain Hildenborough growing syntrophically with Methanococcus maripaludis on lactate were used to develop new and revised models for their alternative electron transfer and energy conservation systems. Lactate oxidation by strain G20 generates a reduced thiol-disulfide redox pair(s) and ferredoxin that are energetically coupled to H ؉ /CO 2 reduction by periplasmic formate dehydrogenase and hydrogenase via a flavin-based reverse electron bifurcation process (electron confurcation) and a menaquinone (MQ) redox loop-mediated reverse electron flow involving the membrane-bound Qmo and Qrc complexes. In contrast, strain Hildenborough uses a larger number of cytoplasmic and periplasmic proteins linked in three intertwining pathways to couple H ؉ reduction to lactate oxidation. The faster growth of strain G20 in coculture is associated with a kinetic advantage conferred by the Qmo-MQ-Qrc loop as an electron transfer system that permits higher lactate oxidation rates under elevated hydrogen levels (thereby enhancing methanogenic growth) and use of formate as the main electron-exchange mediator (>70% electron flux), as opposed to the primarily hydrogen-based exchange by strain Hildenborough. This study further demonstrates the absence of a conserved gene core in Desulfovibrio that would determine the ability for a syntrophic lifestyle. In anoxic environments depleted in inorganic electron acceptors (e.g., freshwater and marine sediments, flooded soils, landfills, and sewage digesters), 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. In these assemblages, sulfate-reducing bacteria (SRB) 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) yields sufficient energy only for cell maintenance and growth when the methanogens maintain low concentrations of the products of SRB metabolism (acetate, hydrogen, and formate) (1-3). As a result, the metabolism of one community member is directly influenced by and dependent upon the activity of the other. Hydrogen and formate are considered the primary shuttle compounds for interspecies electron transfer (1-3). Additionally, single reports suggest the involvement of cysteine or exogenous carriers such as humi...

Correlation between microbial community and granule conductivity in anaerobic bioreactors for brewery wastewater treatment

“…Sulfate reducing bacteria, such as Desulfovibrio and Syntrophobacter spp., were also abundant in many of the UASB reactor samples. Both of these genera are capable of switching between sulfidogenic and syntrophic lifestyles (Meyer et al, 2013). Syntrophobacter species were abundant in twelve granular samples out of fourteen and accounted for 0.64-15.8% of the total community.…”

Carbon cloth stimulates direct interspecies electron transfer in syntrophic co-cultures

“…Desulfovibrio species can grow syntrophically by producing H 2 or formate as interspecies electron carriers (Meyer et al, 2013;Walker et al, 2009). The addition of carbon cloth did not accelerate the metabolism of a co-culture of D. vulgaris and G. sulfurreducens.…”

Roles of HynAB and Ech, the Only Two Hydrogenases Found in the Model Sulfate Reducer Desulfovibrio gigas

“…Also, during syntrophic growth, a similar role of the periplasmic hydrogenase, acting as an H 2 -producing enzyme, was observed in D. vulgaris Hildenborough cultures grown in lactate with a hydrogenotrophic methanogen (8). Furthermore, also in Desulfovibrio alaskensis G20, the HynAB hydrogenase seems to be the main enzyme responsible for H 2 production during syntrophic growth (12).…”

“…In addition, the expression patterns of different hydrogenases were shown to be different and to depend on the substrate, fermentative or respiratory growth, or metal availability (5,(7)(8)(9)(10)(11)(12)(13). Furthermore, the function of each hydrogenase in terms of hydrogen production or oxidation may vary depending on the conditions presented to the cell.…”