Global transcriptomic analysis of Desulfovibrio vulgaris on different electron donors

Zhang, Weiwen; Culley, David E.; Scholten, Johannes C. M.; Hogan, Mike; Vitiritti, Luigi; Brockman, Fred J.

doi:10.1007/s10482-005-9024-z

Cited by 62 publications

(42 citation statements)

References 37 publications

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“…Despite trace concentrations of sulfate in the growth medium, key genes for sulfate respiration (genes encoding ATP sulfurylase, adenylyl-sulfate reductase, dissimilatory sulfite reductase, pyrophosphatase, and thiosulfate reductase) were also upregulated during syntrophic growth, consistent with previous observations of constitutive expression (13,49). However, none of the sulfate permease genes were upregulated, and one (DVU0053) was significantly downregulated.…”

Section: Resultssupporting

confidence: 88%

The Electron Transfer System of Syntrophically Grown Desulfovibrio vulgaris

et al. 2009

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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.

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Section: Resultssupporting

confidence: 88%

The Electron Transfer System of Syntrophically Grown Desulfovibrio vulgaris

et al. 2009

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“…Thus, formate induces higher expression of this enzyme in the presence of both Mo and W, whereas hydrogen leads to a strong increase in expression only in the presence of W, suggesting that the interplay between regulation by the metals and the growth substrates is different for formate relative to lactate or H 2 . Previous microarray experiments have already reported that formate and hydrogen lead to increased expression of the three FDHs in D. vulgaris relative to lactate (34,53). Overall, the qRT-PCR results for the FdhAB fdhB mRNA levels are in agreement with the protein levels and activity results and suggest that tungsten is an inducer of FdhAB gene expression.…”

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confidence: 84%

“…Notably, when cells were grown with formate or hydrogen, there was a very high increase in activity when Mo was replaced with W, and this effect was more pronounced in the soluble fraction than in the membrane fraction. The higher activities of cells grown with formate, and particularly with hydrogen, are in line with the reported higher expression of the D. vulgaris FDH genes during growth with these electron donors than that with lactate (34,53). For these two conditions, we also tested the simultaneous addition of both metals or no addition.…”

Section: Effect Of Mo and W On D Vulgaris Growth And Fdh Activitiessupporting

confidence: 72%

Tungsten and Molybdenum Regulation of Formate Dehydrogenase Expression in Desulfovibrio vulgaris Hildenborough

et al. 2011

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Formate is an important energy substrate for sulfate-reducing bacteria in natural environments, and both molybdenum-and tungsten-containing formate dehydrogenases have been reported in these organisms. In this work, we studied the effect of both metals on the levels of the three formate dehydrogenases encoded in the genome of Desulfovibrio vulgaris Hildenborough, with lactate, formate, or hydrogen as electron donors. Using Western blot analysis, quantitative real-time PCR, activity-stained gels, and protein purification, we show that a metal-dependent regulatory mechanism is present, resulting in the dimeric FdhAB protein being the main enzyme present in cells grown in the presence of tungsten and the trimeric FdhABC 3 protein being the main enzyme in cells grown in the presence of molybdenum. The putatively membrane-associated formate dehydrogenase is detected only at low levels after growth with tungsten. Purification of the three enzymes and metal analysis shows that FdhABC 3 specifically incorporates Mo, whereas FdhAB can incorporate both metals. The FdhAB enzyme has a much higher catalytic efficiency than the other two. Since sulfate reducers are likely to experience high sulfide concentrations that may result in low Mo bioavailability, the ability to use W is likely to constitute a selective advantage.Formate is a key metabolite in anaerobic habitats, arising as a metabolic product of bacterial fermentations and functioning as a growth substrate for many microorganisms (for example, methanogens and sulfate-reducing bacteria [SRB]). Formate is also an intermediate in the energy metabolism of several prokaryotes and a crucial compound in many syntrophic associations, whereby organisms live close to the thermodynamic limit (30,45). Recent reports indicate that formate plays an even more important role in anaerobic microbial metabolism than previously considered (14,24,27). The key enzyme in formate metabolism is formate dehydrogenase (FDH) (50), a member of the dimethyl sulfoxide (DMSO) reductase family. It catalyzes the reversible two-electron oxidation of formate or reduction of CO 2 and plays a role in energy metabolism and carbon fixation. In anaerobic microorganisms, FDH includes a molybdenum or tungsten bis-(pyranopterin guanidine dinucleotide) cofactor and iron-sulfur clusters (20, 41) and shows great variability in quaternary structure, physiological redox partner, and cellular location (7,23,38,50).FDH was the first enzyme shown to naturally incorporate tungsten, at a time when this element was considered to be mostly an antagonist to molybdenum (2, 52). Since then, several tungstoenzymes have been isolated and characterized, mainly but not exclusively from archaeal organisms, including FDHs, formylmethanofuran dehydrogenases (FMDH), aldehyde oxidoreductases (AOR) (not belonging to the xanthine oxidase family), and acetylene hydratase (3,4,20,25,31,41). FDHs and FMDHs can naturally incorporate either tungsten or molybdenum. Since these two elements have very similar chemical and catalytic properties,...

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“…Most recent studies have either failed to find a significant correlation between protein and mRNA abundances (Gygi et al, 1999) or have observed only a weak correlation (Ideker et al, 2001;Greenbaum et al, 2002;Washburn et al, 2003;Zhang et al, 2006b;Nie et al, 2007). It has been suggested that the discrepancy arises from several factors, including protein regulation by post-translational modification, posttranscriptional regulation of protein synthesis, differences in the half-lives of mRNA and proteins, possible functional requirement for protein binding, and significant levels of experimental error (Greenbaum et al, 2002;Beyer et al, 2004;Park et al, 2005).…”

Section: Integrated Transcriptomics and Proteomicsmentioning

confidence: 99%

Integrating multiple ‘omics’ analysis for microbial biology: application and methodologies

Zhang

Li²,

Nie³

2010

Microbiology

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416

241

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Recent advances in various ‘omics’ technologies enable quantitative monitoring of the abundance of various biological molecules in a high-throughput manner, and thus allow determination of their variation between different biological states on a genomic scale. Several popular ‘omics’ platforms that have been used in microbial systems biology include transcriptomics, which measures mRNA transcript levels; proteomics, which quantifies protein abundance; metabolomics, which determines abundance of small cellular metabolites; interactomics, which resolves the whole set of molecular interactions in cells; and fluxomics, which establishes dynamic changes of molecules within a cell over time. However, no single ‘omics’ analysis can fully unravel the complexities of fundamental microbial biology. Therefore, integration of multiple layers of information, the multi-‘omics’ approach, is required to acquire a precise picture of living micro-organisms. In spite of this being a challenging task, some attempts have been made recently to integrate heterogeneous ‘omics’ datasets in various microbial systems and the results have demonstrated that the multi-‘omics’ approach is a powerful tool for understanding the functional principles and dynamics of total cellular systems. This article reviews some basic concepts of various experimental ‘omics’ approaches, recent application of the integrated ‘omics’ for exploring metabolic and regulatory mechanisms in microbes, and advances in computational and statistical methodologies associated with integrated ‘omics’ analyses. Online databases and bioinformatic infrastructure available for integrated ‘omics’ analyses are also briefly discussed.

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Global transcriptomic analysis of Desulfovibrio vulgaris on different electron donors

Cited by 62 publications

References 37 publications

The Electron Transfer System of Syntrophically Grown Desulfovibrio vulgaris

The Electron Transfer System of Syntrophically Grown Desulfovibrio vulgaris

Tungsten and Molybdenum Regulation of Formate Dehydrogenase Expression in Desulfovibrio vulgaris Hildenborough

Integrating multiple ‘omics’ analysis for microbial biology: application and methodologies

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