Influence of tungsten on metabolic patterns in Pyrococcus furiosus, a hyperthermophilic archaeon

Schicho, R. N.; Snowden, Lesley J.; Mukund, Swarnalatha; Park, Jae-Bum; Adams, Michael W. W.; Kelly, Robert M.

doi:10.1007/bf00290921

Cited by 32 publications

(12 citation statements)

References 30 publications

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“…The effect of W on the growth of P. furiosus and on the fermentation of maltose and peptides was subsequently extended to chemostat experiments under energy-limiting conditions [134,135]. These showed that the addition of maltose to a peptidelimited culture increased the cell yields significantly (as measured by dry weight and protein content), but the greatest effect was observed when W was also added.…”

Section: Hyperthermophilesmentioning

confidence: 99%

Tungsten in biological systems

Kletzin

Adams

1996

FEMS Microbiology Reviews

134

144

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Tungsten (atomic number 74) and the chemically analogous and very similar metal molybdenum (atomic number 42) are minor yet equally abundant elements on this planet. The essential role of molybdenum in biology has been known for decades and molybdoenzymes are ubiquitous. Yet, it is only recently that a biological role for tungsten has been established in prokaryotes, although not as yet in eukaryotes. The best characterized organisms with regard to their metabolism of tungsten are certain species of hyperthermophilic archaea (Pyrococcus furiosus and Thermococcus litoralis), methanogens (Methanobacterium thermoautotrophicum and Mb. wolfei), Gram-positive bacteria (Clostridium thermoaceticum, C. formicoaceticum and Eubacterium acidaminophilum), Gram-negative anaerobes (Desulfovibrio gigas and Pelobacter acetylenicus) and Gram-negative aerobes (Methylobacterium sp. RXM). Of these, only the hyperthermophilic archaea appear to be obligately tungsten-dependent. Four different types of tungstoenzyme have been purified: formate dehydrogenase, formyl methanofuran dehydrogenase, acetylene hydratase, and a class of phylogenetically related oxidoreductases that catalyze the reversible oxidation of aldehydes. These are carboxylic reductase, and three ferredoxin-dependent oxidoreductases which oxidize various aldehydes, formaldehyde and glyceraldehyde 3-phosphate. All tungstoenzymes catalyze redox reactions of very low potential (< -420 mV) except one (acetylene hydratase) which catalyzes a hydration reaction. The tungsten in these enzymes is bound by a pterin moiety similar to that found in molybdoenzymes. The first crystal structure of a tungsten-or pterin-containing enzyme, that of aldehyde ferredoxin oxidoreductase from P. furiosus, has revealed a catalytic site with one W atom coordinated to two pterin molecules which are themselves bridged by a magnesium ion. The geochemical, ecological, biochemical and phylogenetic basis for W-vs. Mo-dependent organisms is discussed.

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Section: Hyperthermophilesmentioning

confidence: 99%

Tungsten in biological systems

Kletzin

Adams

1996

FEMS Microbiology Reviews

134

144

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“…In the npED branch, the bifunctional 2-keto-3-deoxy-(6-phospho)-gluconate (KD(P)G) aldolase, which is a key player in both branches, cleaves KDG into pyruvate and glyceraldehyde (Buchanan et al 1999;Lamble et al 2003;Lamble et al 2005;Ahmed et al 2005). Glyceraldehyde is then oxidized to glycerate by glyceraldehyde dehydrogenase Jung and Lee 2006) or glyceraldehyde oxidoreductase (Kardinahl et al 1999;Mukund and Adams 1991;Schicho et al 1993;Selig and Schönheit 1994). The subsequent phosphorylation by glycerate kinase (MOFRL family) results in the formation of 2-phosphoglycerate (Kehrer et al 2007;.…”

Section: Introductionmentioning

confidence: 99%

The non-phosphorylating glyceraldehyde-3-phosphate dehydrogenase (GAPN) of Sulfolobus solfataricus: a key-enzyme of the semi-phosphorylative branch of the Entner–Doudoroff pathway

et al. 2007

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Archaea utilize a branched modification of the classical Entner-Doudoroff (ED) pathway for sugar degradation. The semi-phosphorylative branch merges at the level of glyceraldehyde 3-phosphate (GAP) with the lower common shunt of the Emden-Meyerhof-Parnas pathway. In Sulfolobus solfataricus two different GAP converting enzymes-classical phosphorylating GAP dehydrogenase (GAPDH) and the non-phosphorylating GAPDH (GAPN)-were identified. In Sulfolobales the GAPN encoding gene is found adjacent to the ED gene cluster suggesting a function in the regulation of the semi-phosphorylative ED branch. The biochemical characterization of the recombinant GAPN of S. solfataricus revealed that-like the well-characterized GAPN from Thermoproteus tenax-the enzyme of S. solfataricus exhibits allosteric properties. However, both enzymes show some unexpected differences in co-substrate specificity as well as regulatory fine-tuning, which seem to reflect an adaptation to the different lifestyles of both organisms. Phylogenetic analyses and database searches in Archaea indicated a preferred distribution of GAPN (and/or GAP oxidoreductase) in hyperthermophilic Archaea supporting the previously suggested role of GAPN in metabolic thermoadaptation. This work suggests an important role of GAPN in the regulation of carbon degradation via modifications of the EMP and the branched ED pathway in hyperthermophilic Archaea.Keywords Glyceraldehyde-3-phosphate Á Non-phosphorylating glyceraldehyde-3-phosphate dehydrogenase Á GAPN Á Aldehyde dehydrogenase superfamily Á Branched Entner-Doudoroff pathway Á Carbohydrate metabolism Á Archaea Abbreviations EDEntner-Doudoroff sp Semi-phosphorylative np Non-phosphorylative EMP Embden-Meyerhof-Parnas G1P

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“…The results indicate that maltose and complex carbohydrates are fermented by a novel tungsten-dependent pyroglycolytic pathway (36,45), with H2, CO2, and acetate as the primary products. P. furiosus will also utilize pyruvate as a carbon source, and although S was reported to have no effect on the energetics of pyruvate metabolism (44), these experiments were performed with batch cultures which were not energy limited throughout.…”

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confidence: 95%

Bioenergetics of sulfur reduction in the hyperthermophilic archaeon Pyrococcus furiosus

et al. 1993

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The bioenergetic role of the reduction of elemental sulfur (SO) in the hyperthermophilic archaeon (formerly archaebacterium) Pyrococcusfuriosus was investigated with chemostat cultures with maltose as the limiting carbon source. The maximal yield coefficient was 99.8 g (dry weight) of cells (cdw) per mol of maltose in the presence of So but only 51.3 g (cdw) per mol of maltose if So was omitted. However, the corresponding maintenance coefficients were not found to be significantly different. The primary fermentation products detected were H2, C02, and acetate, together with H2S, when So was also added to the growth medium. If H2S was summed with H2 to represent total reducing equivalents released during fermentation, the presence of So had no significant effect on the pattern of fermentation products. In addition, the presence of So did not significantly affect the specific activities in cell extracts of hydrogenase, sulfur reductase, a-glucosidase, or protease. These results suggest either that So reduction is an energy-conserving reaction, i.e., So respiration, or that So has a stimulatory effect on or helps overcome a process that is yield limiting. A modification of the Entner-Doudoroff glycolytic pathway has been proposed as the primary route of glucose catabolism in P.furiosus (S. Mukund and M. W. W. Adams, J. Biol. Chem. 266:14208-14216, 1991). Operation of this pathway should yield 4 mol of ATP per mol of maltose oxidized, from which one can calculate a value of 12.9 g (cdw)per mol of ATP for non-So growth. Comparison of this value to the yield data for growth in the presence of S0 indicates that So reduction is equivalent to an ATP yield of 0.5 mol of ATP per mol of So reduced. Possible mechanisms to account for this apparent energy conservation are discussed.Microorganisms that are able to grow optimally near the normal boiling point of water are a very recent discovery (48). To date, all have been classified as archaea (formerly archaebacteria [57]). The existence of such organisms has raised many fundamental biological questions. For example, one of the distinguishing growth characteristics of these so-called hyperthermophiles is their ability to reduce elemental sulfur (S) to H2S, and there has been much speculation as to So's physiological role (4, 22, 44) (for reviews, see references 1, 26, 42, and 48). On the other hand, the reduction of S to H2S is extremely limited in nonhyperthermophilic organisms. For example, only the mesophilic (eu) bacterium Desulfuromonas acetoxidans (39) and the moderate thermophile Desulfurella acetivorans (6) are obligately dependent upon the anaerobic respiration of So for growth, and only a few organisms which facultatively reduce So are known (28, 30a, 33, 57a, 58). In contrast, all known hyperthermophiles metabolize SO; in fact, the majority are obligately dependent upon So reduction and use either H2 or organic compounds as electron donors. The best studied is the autotroph Pyrodictium brockii (49), from which several components of its membrane-bound electron tra...

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Influence of tungsten on metabolic patterns in Pyrococcus furiosus, a hyperthermophilic archaeon

Cited by 32 publications

References 30 publications

Tungsten in biological systems

Tungsten in biological systems

The non-phosphorylating glyceraldehyde-3-phosphate dehydrogenase (GAPN) of Sulfolobus solfataricus: a key-enzyme of the semi-phosphorylative branch of the Entner–Doudoroff pathway

Bioenergetics of sulfur reduction in the hyperthermophilic archaeon Pyrococcus furiosus

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