Vacuolar respiration of nitrate coupled to energy conservation in filamentous <i><scp>B</scp>eggiatoaceae</i>

Beutler, Martin; Milucka, Jana; Hinck, Susanne; Schreiber, Frank; Brock, Jörg; Mußmann, Marc; Schulz-Vogt, Heide N.; Beer, Dirk de

doi:10.1111/j.1462-2920.2012.02851.x

Cited by 20 publications

(19 citation statements)

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“…V-type ATPases are common in eukaryotes and archaea but are rarely present in bacteria (Beyenbach and Wieczorek, 2006 ). “ Candidatus Allobeggiatoa,” which contains nitrate storage vacuoles, employs V-type ATPases and PPase to generate ATP by pumping protons into the cytoplasm across the vacuolar membranes (Beutler et al, 2012 ). Alternatively, proton gradients generated by V-type ATPases and PPase at the expense of ATP can be used to drive transport of substrates across vacuolar membranes (Martinoia et al, 2000 ; Beyenbach and Wieczorek, 2006 ) and were proposed to facilitate nitrate uptake in marine Beggiatoa (Mußmann et al, 2007 ).…”

Section: Discussionmentioning

confidence: 99%

Metabolic diversity and ecological niches of Achromatium populations revealed with single-cell genomic sequencing

et al. 2015

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Large, sulfur-cycling, calcite-precipitating bacteria in the genus Achromatium represent a significant proportion of bacterial communities near sediment-water interfaces at sites throughout the world. Our understanding of their potentially crucial roles in calcium, carbon, sulfur, nitrogen, and iron cycling is limited because they have not been cultured or sequenced using environmental genomics approaches to date. We utilized single-cell genomic sequencing to obtain one incomplete and two nearly complete draft genomes for Achromatium collected at Warm Mineral Springs (WMS), FL. Based on 16S rRNA gene sequences, the three cells represent distinct and relatively distant Achromatium populations (91–92% identity). The draft genomes encode key genes involved in sulfur and hydrogen oxidation; oxygen, nitrogen and polysulfide respiration; carbon and nitrogen fixation; organic carbon assimilation and storage; chemotaxis; twitching motility; antibiotic resistance; and membrane transport. Known genes for iron and manganese energy metabolism were not detected. The presence of pyrophosphatase and vacuolar (V)-type ATPases, which are generally rare in bacterial genomes, suggests a role for these enzymes in calcium transport, proton pumping, and/or energy generation in the membranes of calcite-containing inclusions.

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Section: Discussionmentioning

confidence: 99%

Metabolic diversity and ecological niches of Achromatium populations revealed with single-cell genomic sequencing

et al. 2015

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“…Additionally, H 2 S, which can scavenge reactive oxygen species (48), may serve as an extracellular antioxidant under conditions in which sulfide is fluxing into oxygenated waters. Under anoxic conditions, oxidized forms of inorganic nitrogen whether exogenous, or stored within the vacuole, serve as terminal electron acceptors (3, 49). Both Ca.…”

Section: Resultsmentioning

confidence: 99%

Cellular reductase activity in uncultivatedThiomargarita spp. assayed using a redox-sensitive dye

Bailey

Flood

Ricci

et al. 2017

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12The largest known bacteria, Thiomargarita spp., have yet to be isolated in pure culture, but their 13 large size allows for individual cells to be followed in time course experiments, or to be 14 individually sorted for 'omics-based investigations. Here we report a novel application of a 15 tetrazolium-based dye that measures the flux of reductase production from catabolic pathways to 16 investigate the metabolic activity of individual cells of Thiomargarita spp. When coupled to 17 microscopy, staining of the cells with a tetrazolium-formazan dye allows for metabolic responses 18in Thiomargarita spp. to be to be tracked in the absence of observable cell division. Additionally, 19 the metabolic activity of Thiomargarita spp. cells can be differentiated from the metabolism of 20 other microbes in specimens that contain adherent bacteria. The results of our redox-dye-based 21 assay suggests that Thiomargarita is the most metabolically versatile under anoxic conditions 22where it appears to express cellular reductase activity in response to the electron donors 23 succinate, acetate, citrate, formate, thiosulfate, H 2 , and H 2 S. Under hypoxic conditions, formazan 24 staining results suggest the metabolism of succinate, and likely acetate, citrate, and H 2 S. Cells 25 incubated under oxic conditions showed the weakest formazan staining response, and then only 26 to H 2 S, citrate, and perhaps succinate. These results provide experimental validation of recent 27 genomic studies of Ca. Thiomargarita nelsonii that suggest metabolic plasticity and mixotrophic 28 metabolism. The cellular reductase response of bacteria attached to the exteriors of 29Thiomargarita also supports the possibility of trophic interactions between these largest of 30 known bacteria and attached epibionts. 31 IMPORTANCE 32The metabolic potentials of many microorganisms that cannot be grown in the laboratory are 33 known only from genomic data. Genomes of Thiomargarita spp. suggest that these largest of 34 known bacteria are mixotrophs, combining lithotrophic metabolisms with organic carbon 35 degradation. Our use of a redox-sensitive tetrazolium dye to query the metabolism of these 36 bacteria provides an independent line of evidence that corroborates the apparent metabolic 37 plasticity of Thiomargarita observed in recently produced genomes. Finding new cultivation-38 independent means of testing genomic results is critical to testing genome-derived hypotheses on 39 the metabolic potentials of uncultivated microorganisms. 40 41

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“…It is conceivable that the hyphae of An-4 grow in direction of NO 3 - -containing layers closer to the sediment surface to facilitate NO 3 - uptake. Finally, it remains to be investigated whether An-4 accumulates NO 3 - in acidic vacuoles as recently shown for large sulfur bacteria [38] or in the cytosol of the hyphae.…”

Section: Discussionmentioning

confidence: 99%

Dissimilatory nitrate reduction by Aspergillus terreus isolated from the seasonal oxygen minimum zone in the Arabian Sea

et al. 2014

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BackgroundA wealth of microbial eukaryotes is adapted to life in oxygen-deficient marine environments. Evidence is accumulating that some of these eukaryotes survive anoxia by employing dissimilatory nitrate reduction, a strategy that otherwise is widespread in prokaryotes. Here, we report on the anaerobic nitrate metabolism of the fungus Aspergillus terreus (isolate An-4) that was obtained from sediment in the seasonal oxygen minimum zone in the Arabian Sea, a globally important site of oceanic nitrogen loss and nitrous oxide emission.ResultsAxenic incubations of An-4 in the presence and absence of oxygen and nitrate revealed that this fungal isolate is capable of dissimilatory nitrate reduction to ammonium under anoxic conditions. A 15N-labeling experiment proved that An-4 produced and excreted ammonium through nitrate reduction at a rate of up to 175 nmol 15NH4+ g-1 protein h-1. The products of dissimilatory nitrate reduction were ammonium (83%), nitrous oxide (15.5%), and nitrite (1.5%), while dinitrogen production was not observed. The process led to substantial cellular ATP production and biomass growth and also occurred when ammonium was added to suppress nitrate assimilation, stressing the dissimilatory nature of nitrate reduction. Interestingly, An-4 used intracellular nitrate stores (up to 6–8 μmol NO3- g-1 protein) for dissimilatory nitrate reduction.ConclusionsOur findings expand the short list of microbial eukaryotes that store nitrate intracellularly and carry out dissimilatory nitrate reduction when oxygen is absent. In the currently spreading oxygen-deficient zones in the ocean, an as yet unexplored diversity of fungi may recycle nitrate to ammonium and nitrite, the substrates of the major nitrogen loss process anaerobic ammonium oxidation, and the potent greenhouse gas nitrous oxide.

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Vacuolar respiration of nitrate coupled to energy conservation in filamentous Beggiatoaceae

Cited by 20 publications

References 51 publications

Metabolic diversity and ecological niches of Achromatium populations revealed with single-cell genomic sequencing

Metabolic diversity and ecological niches of Achromatium populations revealed with single-cell genomic sequencing

Cellular reductase activity in uncultivatedThiomargarita spp. assayed using a redox-sensitive dye

Dissimilatory nitrate reduction by Aspergillus terreus isolated from the seasonal oxygen minimum zone in the Arabian Sea

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