Intermediate instability at high temperature leads to low pathway efficiency for an in vitro reconstituted system of gluconeogenesis in Sulfolobus solfataricus

FEBS Journal

Volumn 280, Issue 18, 2013, Pages 4666-4680

  Kouril, Theresa ^a   Esser, Dominik ^a   Kort, Julia ^a   Westerhoff, Hans V ^b,c,d   Siebers, Bettina ^a   Snoep, Jacky L ^b,c,e  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

^e STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

carbon loss; mathematical model; thermal instability; thermophile

Indexed keywords

1,3 DIPHOSPHOGLYCERIC ACID; ADENOSINE TRIPHOSPHATE; BACTERIAL ENZYME; DIHYDROXYACETONE PHOSPHATE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLUCOSE DEHYDROGENASE; GLYCERALDEHYDE 3 PHOSPHATE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; PHOSPHOGLYCERATE KINASE; PYRUVATE KINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TRIOSEPHOSPHATE ISOMERASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYMATIC DEGRADATION; ENZYME ACTIVITY; ENZYME PURIFICATION; ENZYME SYNTHESIS; GLUCONEOGENESIS; HALF LIFE TIME; HIGH TEMPERATURE; IN VITRO STUDY; MATHEMATICAL MODEL; NONHUMAN; PRIORITY JOURNAL; SULFOLOBUS SOLFATARICUS; TEMPERATURE SENSITIVITY; THERMAL INSTABILITY; THERMOSTABILITY;

CARBON LOSS; MATHEMATICAL MODEL; THERMAL INSTABILITY; THERMOPHILE;

ARCHAEAL PROTEINS; DIHYDROXYACETONE PHOSPHATE; DIPHOSPHOGLYCERIC ACIDS; ENZYME STABILITY; ESCHERICHIA COLI; FRUCTOSE-BISPHOSPHATE ALDOLASE; FRUCTOSEPHOSPHATES; GLUCONEOGENESIS; GLYCERALDEHYDE 3-PHOSPHATE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; GLYCERIC ACIDS; HALF-LIFE; HOT TEMPERATURE; KINETICS; MODELS, STATISTICAL; PHOSPHOGLYCERATE KINASE; RECOMBINANT PROTEINS; SULFOLOBUS SOLFATARICUS; THERMODYNAMICS; TRIOSE-PHOSPHATE ISOMERASE;

SULFOLOBUS SOLFATARICUS;

EID: 84883448144     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12438     Document Type: Article

References (41)

1. Stetter KO, (1999) Extremophiles and their adaptation to hot environments. FEBS Lett 452, 22-25.
2. Daniel RM, &, Cowan DA, (2000) Biomolecular stability and life at high temperatures. Cell Mol Life Sci 57, 250-264.
3. Kawashima T, Amano N, Koike H, Makino SI, Higuchi S, Kawashima-Ohya Y, Watanabe K, Yamazaki M, Kanehori K, Kawamoto T, et al,. (2000) Archaeal adaptation to higher temperatures revealed by genomic sequence of Thermoplasma volcanium. Proc Natl Acad Sci USA 97, 14257-14262.
4. Kouril T, Kolodkin A, Zaparty M, Steuer R, Ruoff P, Westerhoff HV, Snoep JL, Siebers B, &, consortium, SulfoSYS, (2012) Sulfolobus Systems Biology: Cool Hot Design for Metabolic Pathways. Horizon Scientific Press and Caister Academic Press, Norwich.
5. Imanaka T, &, Atomi H, (2002) Catalyzing 'hot' reactions: enzymes from hyperthermophilic archaea. Chem Rec 2, 149-163.
6. Schramm A, Kohlhoff M, &, Hensel R, (2001) Triose-phosphate isomerase from Pyrococcus woesei and Methanothermus fervidus. Meth Enzymol 331, 62-77.
7. Ahmed H, Ettema TJG, Tjaden B, Geerling ACM, Van Der Oost J, &, Siebers B, (2005) The semi-phosphorylative Entner-Doudoroff pathway in hyperthermophilic archaea: a re-evaluation. Biochem J 390, 529-540.
8. +-dependent glyceraldehyde-3-phosphate dehydrogenase from Thermoproteus tenax. J Biol Chem 273, 6149-6156.
9. Brunner NA, Siebers B, &, Hensel R, (2001) Role of two different glyceraldehyde-3-phosphate dehydrogenases in controlling the reversible Embden-Meyerhof-Parnas pathway in Thermoproteus tenax: regulation on protein and transcript level. Extremophiles 5, 101-109.
10. Lorentzen E, Hensel R, Knura T, Ahmed H, &, Pohl E, (2004) Structural basis of allosteric regulation and substrate specificity of the non-phosphorylating glyceraldehyde 3-phosphate dehydrogenase from Thermoproteus tenax. J Mol Biol 341, 815-828.
11. Ettema TJG, Ahmed H, Geerling ACM, Van Der Oost J, &, Siebers B, (2008) The non-phosphorylating glyceraldehyde-3-phosphate dehydrogenase (gapn) of Sulfolobus solfataricus: a key-enzyme of the semi-phosphorylative branch of the Entner-Doudoroff pathway. Extremophiles 12, 75-88.
12. Zaparty M, Zaigler A, Stamme C, Soppa J, Hensel R, &, Siebers B, (2008) DNA microarray analysis of the central carbohydrate metabolism: glycolytic/gluconeogenic carbon switch in the hyperthermophilic crenarchaeum Thermoproteus tenax. J Bacteriol 190, 2231-2238.
13. Say RF, &, Fuchs G, (2010) Fructose 1,6-bisphosphate aldolase/phosphatase may be an ancestral gluconeogenic enzyme. Nature 464, 1077-1081.
14. Matsubara K, Yokooji Y, Atomi H, &, Imanaka T, (2011) Biochemical and genetic characterization of the three metabolic routes in Thermococcus kodakarensis linking glyceraldehyde 3-phosphate and 3-phosphoglycerate. Mol Microbiol 81, 1300-1312.
15. Zillig W, Stetter KO, &, Wunderl S, (1980) The Sulfolobus- 'Caldariella' group: taxonomy on the basis of the structure of DNA-dependent RNA polymerases. Arch Microbiol 125, 259-269.
16. Albers SV, Birkeland NK, Driessen AJM, Gertig S, Haferkamp P, Klenk HP, Kouril T, Manica A, Pham TK, Ruoff P, et al,. (2009) Sulfosys (sulfolobus systems biology): towards a silicon cell model for the central carbohydrate metabolism of the archaeon Sulfolobus solfataricus under temperature variation. Biochem Soc Trans 37, 58-64.
17. Lamble HJ, Heyer NI, Bull SD, Hough DW, &, Danson MJ, (2003) Metabolic pathway promiscuity in the archaeon Sulfolobus solfataricus revealed by studies on glucose dehydrogenase and 2-keto-3-deoxygluconate aldolase. J Biol Chem 278, 34066-34072.
18. Lamble HJ, Theodossis A, Milburn CC, Taylor GL, Bull SD, Hough DW, &, Danson MJ, (2005) Promiscuity in the part-phosphorylative Entner-Doudoroff pathway of the archaeon Sulfolobus solfataricus. FEBS Lett 579, 6865-6869.
19. Snijders APL, Walther J, Peter S, Kinnman I, De Vos MGJ, Van De Werken HJG, Brouns SJJ, Van Der Oost J, &, Wright PC, (2006) Reconstruction of central carbon metabolism in Sulfolobus solfataricus using a two-dimensional gel electrophoresis map, stable isotope labelling and DNA microarray analysis. Proteomics 6, 1518-1529.
20. Van Der Oost J, &, Siebers B, (2007) The Glycolytic Pathways of Archaea: Evolution by Tinkering. Vol. 1, pp. 247-259. Blackwell Publishing, Singapore.
21. Zaparty M, &, Siebers B, (2011) Reconstruction of the central carbon metabolic network of thermoacidophilic Archaea. In Physiology, Metabolism and Enzymology of Thermoacidophiles (Horikoshi K, ed). Vol. 1, pp. 602-639. Springer, Tokyo.
22. Potters MB, Solow BT, Bischoff KM, Graham DE, Lower BH, Helm R, &, Kennelly PJ, (2003) Phosphoprotein with phosphoglycerate mutase activity from the archaeon Sulfolobus solfataricus. J Bacteriol 185, 2112-2121.
23. Dello Russo A, Rullo R, Masullo M, Ianniciello G, Arcari P, &, Bocchini V, (1995) Glyceraldehyde-3-phosphate dehydrogenase in the hyperthermophilic archaeon Sulfolobus solfataricus: characterization and significance in glucose metabolism. Biochem Mol Biol Int 36, 123-135.
24. Hess D, Kruger K, Knappik A, Palm P, &, Hensel R, (1995) Dimeric 3-phosphoglycerate kinases from hyperthermophilic archaea. Cloning, sequencing and expression of the 3-phosphoglycerate kinase gene of Pyrococcus woesei in Escherichia coli and characterization of the protein. Structural and functional comparison with the 3-phosphoglycerate kinase of Methanothermus fervidus. Eur J Biochem 233, 227-237.
25. Jones CE, Fleming TM, Cowan DA, Littlechild JA, &, Piper PW, (1995) The phosphoglycerate kinase and glyceraldehyde-3-phosphate dehydrogenase genes from the thermophilic archaeon Sulfolobus solfataricus overlap by 8 bp-isolation, sequencing of the genes and expression in Escherichia coli. Eur J Biochem 233, 800-808.
26. Du J, Say RF, Lu W, Fuchs G, &, Einsle O, (2011) Active-site remodelling in the bifunctional fructose-1,6-bisphosphate aldolase/phosphatase. Nature 478, 534-537.
27. Fushinobu S, Nishimasu H, Hattori D, Song HJ, &, Wakagi T, (2011) Structural basis for the bifunctionality of fructose-1,6-bisphosphate aldolase/phosphatase. Nature 478, 538-541.
28. König H, Skorko R, Zillig W, &, Reiter WD, (1982) Glycogen in thermoacidophilic archaebacteria of the genera Sulfolobus, Thermoproteus, Desulfurococcus and Thermococcus. Arch Microbiol 132, 297-303.
29. Maruta K, Mitsuzumi H, Nakada T, Kubota M, Chaen H, Fukuda S, Sugimoto T, &, Kurimoto M, (1996) Cloning and sequencing of a cluster of genes encoding novel enzymes of trehalose biosynthesis from thermophilic archaebacterium Sulfolobus acidocaldarius. Biochim Biophys Acta (BBA) General Subjects 1291, 177-181.
30. Park HS, Park JT, Kang HK, Cha H, Kim DS, Kim JW, &, Park KH, (2007) TreX from Sulfolobus solfataricus ATCC 35092 displays isoamylase and 4-α-glucanotransferase activities. Biosci Biotechnol Biochem 71, 1348-1352.
31. Woo EJ, Lee S, Cha H, Park JT, Yoon SM, Song HN, &, Park KH, (2008) Structural insight into the bifunctional mechanism of the glycogen-debranching enzyme TreX from the archaeon Sulfolobus solfataricus. J Biol Chem 283, 28641-28648.
32. Hofmeyr JH, &, Cornish-Bowden A, (1997) The reversible Hill equation: how to incorporate cooperative enzymes into metabolic models. Cabios 13, 377-385.
33. Hanekom AJ (2006) Generic rate equations for modelling multisubstrate reactions in computational systems biology. Master's thesis, Stellenbosch University, South Africa.
34. Ito F, Chishiki H, Fushinobu S, &, Wakagi T, (2012) Comparative analysis of two glyceraldehyde-3-phosphate dehydrogenases from a thermoacidophilic archaeon, Sulfolobus tokodaii. FEBS Lett 586, 3097-3103.
35. Siebers B, Tjaden B, Michalke K, Dörr C, Ahmed H, Zaparty M, Gordon P, Sensen CW, Zibat A, &, Klenk HP, et al,. (2004) Reconstruction of the central carbohydrate metabolism of Thermoproteus tenax by use of genomic and biochemical data. J Bacteriol 186, 2179-2194.
36. Dörr C, Zaparty M, Tjaden B, Brinkmann H, &, Siebers B, (2003) The hexokinase of the hyperthermophile Thermoproteus tenax: ATP-dependent hexokinases and ADP-dependent glucokinases, two alternatives for glucose phosphorylation in archaea. J Biol Chem 278, 18744-18753.
37. Hansen T, Schlichting B, &, Schönheit P, (2002) 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.
38. Haferkamp P, Kutschki S, Treichel J, Hemeda H, Sewczyk K, Hoffmann D, Zaparty M, &, Siebers B, (2011) An additional glucose dehydrogenase from Sulfolobus solfataricus: fine-tuning of sugar degradation? Biochem Soc Trans 39, 77-81.
39. Haferkamp P, (2011) Biochemical studies of enzymes involved in glycolysis of the thermoacidophilic crenarchaeon Sulfolobus solfataricus. PhD thesis, University of Duisburg-Essen, Germany.
40. Littlechild JA, &, Isupov M, (2001) Glyceraldehyde-3-phosphate dehydrogenase from Sulfolobus solfataricus. In Methods in Enzymology, Vol. 331: Hyperthermophilic Enzymes, Part B (, Michael WW, &, Adams RMK, eds), pp. 105-117. Academic Press, San Diego, CA.
41. Wolfram Research Inc. (2010) Mathematica Edition: Version 8.0. Wolfram Research Inc., Champaign, IL.