Metabolism of H2 by Desulfovibrio alaskensis G20 during syntrophic growth on lactate

Li, Xiangzhen; McInerney, Michael J.; Stahl, David A.; Krumholz, Lee R.

doi:10.1099/mic.0.051284-0

Cited by 27 publications

(30 citation statements)

References 37 publications

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“…Therefore, Qrc was suggested to link the periplasmic enzymes to the quinone pool by acting as a TpIc 3 : menaquinone oxidoreductase during respiratory growth on H 2 / formate (22,28,62). Recently, its essential function in syntrophy was proposed on the basis of growth defects of qrcB and cycA transposon mutants in coculture (19). The higher redox potential of the MQ relative to the H ϩ /H 2 and CO 2 /formate redox pairs requires a second energy input to efficiently drive the electron flow from the MQ pool (Ϫ80 mV [12,29]) to the periplasmic hydrogenases and formate dehydrogenases via the membrane-bound Qrc complex and TpIc 3 (heme c group redox potentials in D. vulgaris strain Hildenborough, ϩ80 to Ϫ110 mV and Ϫ325 to Ϫ170 mV, respectively [28]).…”

Section: Discussionmentioning

confidence: 99%

“…So far, most biochemical and genetic studies have focused on the investigation of the electron transfer and energy conservation mechanisms in propionate and butyrate oxidizers, e.g., Syntrophobacter and Syntrophomonas (3,5,6,10,11), while there is only limited understanding of the syntrophic metabolism of other representative bacterial species, e.g., Desulfovibrio (17)(18)(19).…”

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

Meyer

Kuehl

Deutschbauer

et al. 2012

Journal of Bacteriology

102

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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...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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

Meyer

Kuehl

Deutschbauer

et al. 2012

Journal of Bacteriology

102

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“…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.…”

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

et al. 2013

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Sulfate-reducing bacteria are characterized by a high number of hydrogenases, which have been proposed to contribute to the overall energy metabolism of the cell, but exactly in what role is not clear. Desulfovibrio spp. can produce or consume H 2 when growing on organic or inorganic substrates in the presence or absence of sulfate. Because of the presence of only two hydrogenases encoded in its genome, the periplasmic HynAB and cytoplasmic Ech hydrogenases, Desulfovibrio gigas is an excellent model organism for investigation of the specific function of each of these enzymes during growth. In this study, we analyzed the physiological response to the deletion of the genes that encode the two hydrogenases in D. gigas, through the generation of ⌬echBC and ⌬hynAB single mutant strains. These strains were analyzed for the ability to grow on different substrates, such as lactate, pyruvate, and hydrogen, under respiratory and fermentative conditions. Furthermore, the expression of both hydrogenase genes in the three strains studied was assessed through quantitative reverse transcription-PCR. The results demonstrate that neither hydrogenase is essential for growth on lactate-sulfate, indicating that hydrogen cycling is not indispensable. In addition, the periplasmic HynAB enzyme has a bifunctional activity and is required for growth on H 2 or by fermentation of pyruvate. Therefore, this enzyme seems to play a dominant role in D. gigas hydrogen metabolism. Hydrogenases are key enzymes in the hydrogen metabolism of Desulfovibrio spp. that catalyze the reversible oxidation of molecular hydrogen into protons and electrons (1). However, their role during sulfate respiration has not been clearly established. Odom and Peck proposed a hydrogen cycling model to explain energy conservation during growth on lactate and sulfate by Desulfovibrio spp., which belong to the deltaproteobacteria subgroup of the sulfate-reducing bacteria (SRB) (2). The model predicts that protons and electrons produced in the oxidation of lactate are used for the production of molecular hydrogen by a cytoplasmic hydrogenase. This hydrogen then diffuses across the membrane to the periplasm, where it is reoxidized by a periplasmic hydrogenase. Electrons are transferred back to the cytoplasm for sulfate reduction, thus creating a proton gradient across the membrane that leads to ATP formation. In this model, the presence of at least two hydrogenases on opposite sides of the membrane is a requirement for growth. In contrast, other studies suggested that the physiological role of these enzymes was to regulate the redox potential of the cell, controlling the flow of protons and electrons and generating a proton motive force (3). More recent models, proposed for Desulfovibrio vulgaris, suggested dual pathways for electron transfer from lactate to sulfate, one involving the cycling of H 2 and the other a route involving a membrane-associated electron transfer chain (4, 5). Several membrane complexes have been identified in SRB that could be involved in this proce...

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“…To date, syntrophic organisms have been shown to be either strictly fermentative (e.g., Syntrophus aciditrophicus and Syntrophomonas wolfei) or those capable of syntrophy in the absence of a terminal electron-accepting process (e.g., Geobacter and Desulfovibrio) (9,16). The electron-accepting organisms are often methanogens (3), but sulfate-reducing (16) and fumarate-reducing organisms (9) have been shown to function efficiently with H 2 and/or formate-producing syntrophic metabolizers.…”

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Syntrophic Growth of Desulfovibrio alaskensis Requires Genes for H ₂ and Formate Metabolism as Well as Those for Flagellum and Biofilm Formation

Krumholz

Bradstock

Sheik

et al. 2015

Appl Environ Microbiol

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In anaerobic environments, mutually beneficial metabolic interactions between microorganisms (syntrophy) are essential for oxidation of organic matter to carbon dioxide and methane. Syntrophic interactions typically involve a microorganism degrading an organic compound to primary fermentation by-products and sources of electrons (i.e., formate, hydrogen, or nanowires) and a partner producing methane or respiring the electrons via alternative electron accepting processes. Using a transposon gene mutant library of the sulfate-reducing Desulfovibrio alaskensis G20, we screened for mutants incapable of serving as the electron-accepting partner of the butyrate-oxidizing bacterium, Syntrophomonas wolfei. A total of 17 gene mutants of D. alaskensis were identified as incapable of serving as the electron-accepting partner. The genes identified predominantly fell into three categories: membrane surface assembly, flagellum-pilus synthesis, and energy metabolism. Among these genes required to serve as the electron-accepting partner, the glycosyltransferase, pilus assembly protein (tadC), and flagellar biosynthesis protein showed reduced biofilm formation, suggesting that each of these components is involved in cell-to-cell interactions. Energy metabolism genes encoded proteins primarily involved in H 2 uptake and electron cycling, including a rhodanese-containing complex that is phylogenetically conserved among sulfate-reducing Deltaproteobacteria. Utilizing an mRNA sequencing approach, analysis of transcript abundance in wild-type axenic and cocultures confirmed that genes identified as important for serving as the electronaccepting partner were more highly expressed under syntrophic conditions. The results imply that sulfate-reducing microorganisms require flagellar and outer membrane components to effectively couple to their syntrophic partners; furthermore, H 2 metabolism is essential for syntrophic growth of D. alaskensis G20.A naerobic oxidation of organic compounds, such as alcohols and fatty acids, is thermodynamically unfavorable when protons or carbon dioxide are used as the electron acceptor, unless the H 2 partial pressure or formate concentration, respectively, can be maintained at extremely low concentrations (1). Thus, complete degradation of organic matter in methanogenic and some other anaerobic systems requires a microbial consortium composed of two or more microbial species to oxidize the carbon and subsequently remove hydrogen (2-5). This synergistic interaction between different microorganisms is defined as syntrophy. The term was first coined in anaerobic, sulfur-oxidizing phototrophic cocultures (6) but was experimentally verified when the methanogenic, archaean Methanobacterium bryantii strain MOH was separated from an ethanol-oxidizing partner, both of which were present in a culture called Methanobacillus omelianskii, which at the time was believed to be a pure culture (7). This work established the general syntrophic model of two microorganisms mutualistically cooperating by transferring electron...

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Metabolism of H2 by Desulfovibrio alaskensis G20 during syntrophic growth on lactate

Cited by 27 publications

References 37 publications

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

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

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

Syntrophic Growth of Desulfovibrio alaskensis Requires Genes for H ₂ and Formate Metabolism as Well as Those for Flagellum and Biofilm Formation

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Metabolism of H2 by Desulfovibrio alaskensis G20 during syntrophic growth on lactate

Cited by 27 publications

References 37 publications

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

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

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

Syntrophic Growth of Desulfovibrio alaskensis Requires Genes for H 2 and Formate Metabolism as Well as Those for Flagellum and Biofilm Formation

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Syntrophic Growth of Desulfovibrio alaskensis Requires Genes for H ₂ and Formate Metabolism as Well as Those for Flagellum and Biofilm Formation