Abstract
Recently, unusual non-regulated ATP-dependent 6-phosphofructokinases (PFK) that belong to the PFK-B family have been described for the hyperthermophilic archaea Desulfurococcus amylolyticus and Aeropyrum pernix. Putative homologues were found in genomes of several archaea including the hyperthermophilic archaeon Methanocaldococcus jannaschii. In this organism, open reading frame MJ0406 had been annotated as a PFK-B sugar kinase. The gene encoding MJ0406 was cloned and functionally expressed in Escherichia coli. The purified recombinant enzyme is a homodimer with an apparent molecular mass of 68 kDa composed of 34 kDa subunits. With a temperature optimum of 85°C and a melting temperature of 90°C, the M. jannaschii nucleotide kinase represents one of the most thermoactive and thermostable members of the PFK-B family described so far. The recombinant enzyme was characterized as a functional nucleoside kinase rather than a 6-PFK. Inosine, guanosine, and cytidine were the most effective phosphoryl acceptors. Besides, adenosine, thymidine, uridin and xanthosine were less efficient. Extremely low activity was found with fructose-6-phosphate. Further, the substrate specificity of closely related PFK-Bs from D. amylolyticus and A. pernix were reanalysed.
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Bork P, Sander C, Valencia A (1993) Convergent evolution of similar enzymatic function on different protein folds: the hexokinase, ribokinase, and galactokinase families of sugar kinases. Protein Sci 2:31–40
Brunner NA, Brinkmann H, Siebers B, Hensel R (1998) NAD+-dependent glyceraldehyde-3-phosphate dehydrogenase from Thermoproteus tenax. The first identified archaeal member of the aldehyde dehydrogenase superfamily is a glycolytic enzyme with unusual regulatory properties. J Biol Chem 273:6149–6156
Bult CJ, White O, Olsen GJ, Zhou L, Fleischmann RD, Sutton GG, Blake JA, Fitzgerald LM, Clayton RA, Gocayne JD, Kerlavage AR, Dougherty BA, Tomb JF, Adams MD, Reich CI, Overbeek R, Kirkness EF, Weinstock KG, Merrick JM, Glodek A, Scott JL, Geoghagen NSM, Venter JC (1996) Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273:1058–1073
Ding Y-HR, Ronimus RS, Morgan HW (2000) Sequencing, cloning, and high-level expression of the pfp gene, encoding a PP i -dependent phosphofructokinase from the extremely thermophilic eubacterium Dictyoglomus thermophilum. J Bacteriol 182:4661–4666
Ding YH, Ronimus RS, Morgan HW (2001) Thermotoga maritima phosphofructokinases: expression and characterization of two unique enzymes. J Bacteriol 183:791–794
Hansen T, Musfeldt M, Schönheit P (2002a) ATP-dependent 6-phosphofructokinase from the hyperthermophilic bacterium Thermotoga maritima: characterization of an extremely thermophilic, allosterically regulated enzyme. Arch Microbiol 177:401–409
Hansen T, Oehlmann M, Schönheit P (2001) Novel type of glucose-6-phosphate isomerase in the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 183:3428–3435
Hansen T, Reichstein B, Schmid R, Schönheit P (2002b) The first archaeal ATP-dependent glucokinase, from the hyperthermophilic crenarchaeon Aeropyrum pernix, represents a monomeric, extremely thermophilic ROK glucokinase with broad hexose specificity. J Bacteriol 184:5955–5965
Hansen T, Schlichting B, Schönheit P (2002c) Glucose-6-phosphate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima: expression of the g6pd gene and characterization of an extremely thermophilic enzyme. FEMS Microbiol Lett 216:249–253
Hansen T, Schönheit P (2000) Purification and properties of the first-identified, archaeal, ATP-dependent 6-phosphofructokinase, an extremely thermophilic non-allosteric enzyme, from the hyperthermophile Desulfurococcus amylolyticus. Arch Microbiol 173:103–109
Hansen T, Schönheit P (2001) Sequence, expression, and characterization of the first archaeal ATP-dependent 6-phosphofructokinase, a non-allosteric enzyme related to the phosphofructokinase-B sugar kinase family, from the hyperthermophilic crenarchaeote Aeropyrum pernix. Arch Microbiol 177:62–69
Hansen T, Schönheit P (2004) ADP-dependent 6-phosphofructokinase, an extremely thermophilic, non-allosteric enzyme from the hyperthermophilic, sulfate-reducing archaeon Archaeoglobus fulgidus strain 7324. Extremophiles 8:29–35
Hansen T, Urbanke C, Schönheit P (2004) Bifunctional phosphoglucose/phosphomannose isomerase from the hyperthermophilic archaeon Pyrobaculum aerophilum. Extremophiles 8:507–512
Holmes ML, Scopes RK, Moritz RL, Simpson RJ, Englert C, Pfeifer F, Dyall-Smith ML (1997) Purification and analysis of an extremely halophilic beta-galactosidase from Haloferax alicantei. Biochim Biophys Acta 1337:276–286
Kengen SW, de Bok FA, van Loo ND, Dijkema C, Stams AJ, De Vos WM (1994) Evidence for the operation of a novel Embden-Meyerhof pathway that involves ADP-dependent kinases during sugar fermentation by Pyrococcus furiosus. J Biol Chem 269:17537–17541
Kengen SW, Tuininga JE, Verhees CH, Van der Oost J, Stams AJ, De Vos WM (2001) ADP-dependent glucokinase and phosphofructokinase from Pyrococcus furiosus. Methods Enzymol 331:41–53
Labes A, Schönheit P (2001) Sugar utilization in the hyperthermophilic, sulfate-reducing archaeon Archaeoglobus fulgidus strain 7324: starch degradation to acetate and CO2 via a modified Embden-Meyerhof pathway and acetyl-CoA synthetase (ADP-forming). Arch Microbiol 176:329–338
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Li MH, Kwok F, Chang WR, Lau CK, Zhang JP, Lo SC, Jiang T, Liang DC (2002) Crystal structure of brain pyridoxal kinase, a novel member of the ribokinase superfamily. J Biol Chem 277:46385–46390
Liacouras AS, Anderson EP (1975) Uridine-cytidine kinase. Purification from a murine neoplasm and characterization of the enzyme. Arch Biochem Biophys 168:66–73
Long MC, Escuyer V, Parker WB (2003) Identification and characterization of a unique adenosine kinase from Mycobacterium tuberculosis. J Bacteriol 185:6548–6555
Mathews II, Erion MD, Ealick SE (1998) Structure of human adenosine kinase at 1.5 Å resolution. Biochemistry 37:15607–15620
Mizote T, Tsuda M, Smith DD, Nakayama H, Nakazawa T (1999) Cloning and characterization of the thiD/J gene of Escherichia coli encoding a thiamin-synthesizing bifunctional enzyme, hydroxymethylpyrimidine kinase/phosphomethylpyrimidine kinase. Microbiology 145:495–501
Mori H, Iida A, Teshiba S, Fujio T (1995) Cloning of a guanosine-inosine kinase gene of Escherichia coli and characterization of the purified gene product. J Bacteriol 177:4921–4926
Ohshima N, Inagaki E, Yasuike K, Takio K, Tahirov TH (2004) Structure of Thermus thermophilus 2-Keto-3-deoxy-gluconate kinase: evidence for recognition of an open chain substrate. J Mol Biol 340:477–489
Qu Q, Lee SJ, Boos W (2004) Molecular and biochemical characterization of a fructose-6-phosphate-forming and ATP-dependent fructokinase of the hyperthermophilic archaeon Thermococcus litoralis. Extremophiles 8:301–308
Ronimus RS, de Heus E, Morgan HW (2001a) Sequencing, expression, characterisation and phylogeny of the ADP-dependent phosphofructokinase from the hyperthermophilic, euryarchaeal Thermococcus zilligii. Biochim Biophys Acta 1517:384–391
Ronimus RS, Kawarabayasi Y, Kikuchi H, Morgan HW (2001b) Cloning, expression and characterisation of a family B ATP-dependent phosphofructokinase activity from the hyperthermophilic crenarchaeon Aeropyrum pernix. FEMS Microbiol Lett 202:85–90
Ronimus RS, Koning J, Morgan HW (1999) Purification and characterization of an ADP-dependent phosphofructokinase from Thermococcus zilligii. Extremophiles 3:121–129
Ronimus RS, Morgan HW (2001) The biochemical properties and phylogenies of phosphofructokinases from extremophiles. Extremophiles 5:357–373
Ronimus RS, Morgan HW (2003) Distribution and phylogenies of enzymes of the Embden-Meyerhof-Parnas pathway from archaea and hyperthermophilic bacteria support a gluconeogenic origin of metabolism. Archaea 1:199–221
Sakuraba H, Yoshioka I, Koga S, Takahashi M, Kitahama Y, Satomura T, Kawakami R, Ohshima T (2002) ADP-dependent glucokinase/phosphofructokinase, a novel bifunctional enzyme from the hyperthermophilic archaeon Methanococcus jannaschii. J Biol Chem 277:12495–12498
Schumacher MA, Scott DM, Mathews II, Ealick SE, Roos DS, Ullman B, Brennan RG (2000) Crystal structures of Toxoplasma gondii adenosine kinase reveal a novel catalytic mechanism and prodrug binding. J Mol Biol 298:875–893
Selig M, Xavier KB, Santos H, Schönheit P (1997) Comparative analysis of Embden-Meyerhof and Entner-Doudoroff glycolytic pathways in hyperthermophilic archaea and the bacterium Thermotoga. Arch Microbiol 167:217–232
Siebers B, Hensel R (2001) Pyrophosphate-dependent phosphofructokinase from Thermoproteus tenax. Methods Enzymol 331:54–62
Siebers B, Tjaden B, Michalke K, Dörr C, Ahmed H, Zaparty M, Gordon P, Sensen CW, Zibat A, Klenk HP, Schuster SC, Hensel R (2004) Reconstruction of the central carbohydrate metabolism of Thermoproteus tenax by use of genomic and biochemical data. J Bacteriol 186:2179–2194
Siebers B, Schönheit P (2005) Unusual pathways and enzymes of central carbohydrate metabolism in archaea. Curr Opin Microbiol 8:695–705
Sigrell JA, Cameron AD, Jones TA, Mowbray SL (1998) Structure of Escherichia coli ribokinase in complex with ribose and dinucleotide determined to 1.8 Å resolution: insights into a new family of kinase structures. Structure 6:183–193
Stetter KO (1996) Hyperthermophilic procaryotes. FEMS Microbiol Rev 18:149–158
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Tuininga JE, Verhees CH, Van der Oost J, Kengen SW, Stams AJ, De Vos WM (1999) Molecular and biochemical characterization of the ADP-dependent phosphofructokinase from the hyperthermophilic archaeon Pyrococcus furiosus. J Biol Chem 274:21023–21028
Usuda Y, Kawasaki H, Shimaoka M, Utagawa T (1997) Characterization of guanosine kinase from Brevibacterium acetylicum ATCC 953. Biochim Biophys Acta 1341:200–206
Van Rompay AR, Norda A, Linden K, Johansson M, Karlsson A (2001) Phosphorylation of uridine and cytidine nucleoside analogs by two human uridine-cytidine kinases. Mol Pharmacol 59:1181–1186
Verhees CH, Kengen SW, Tuininga JE, Schut GJ, Adams MW, De Vos WM, Van der Oost J (2003) The unique features of glycolytic pathways in archaea. Biochem J 375:231–246
Verhees CH, Tuininga JE, Kengen SW, Stams AJ, Van der Oost J, De Vos WM (2001) ADP-dependent phosphofructokinases in mesophilic and thermophilic methanogenic archaea. J Bacteriol 183:7145–7153
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The expert technical assistance of K. Lutter-Mohr and M. Kusche is gratefully acknowledged.
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Communicated by G. Antranikian
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Hansen, T., Arnfors, L., Ladenstein, R. et al. The phosphofructokinase-B (MJ0406) from Methanocaldococcus jannaschii represents a nucleoside kinase with a broad substrate specificity. Extremophiles 11, 105–114 (2007). https://doi.org/10.1007/s00792-006-0018-1
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DOI: https://doi.org/10.1007/s00792-006-0018-1