Unraveling the function of the two Entner-Doudoroff branches in the thermoacidophilic Crenarchaeon Sulfolobus solfataricus P2

FEBS Journal

Volumn 280, Issue 4, 2013, Pages 1126-1138

  Kouril, Theresa ^a   Wieloch, Patricia ^b   Reimann, Julia ^c   Wagner, Michaela ^c   Zaparty, Melanie ^d   Albers, Sonja Verena ^c   Schomburg, Dietmar ^b   Ruoff, Peter ^e   Siebers, Bettina ^a  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

^b TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^c MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^d UNIVERSITY OF REGENSBURG   (Germany)

^e UNIVERSITY OF STAVANGER   (Norway)

Author keywords

carbohydrate metabolism; Entner Doudoroff pathway; glycerate kinase; metabolomics; thermophiles

Indexed keywords

2 KETO 3 DEOXYGLUCONATE KINASE; 5 METHYLADENOSINE; ADENOSINE DERIVATIVE; BACTERIAL ENZYME; FRUCTOSE 6 PHOSPHATE; FUMARIC ACID; GLUCOSE 6 PHOSPHATE; GLYCERATE KINASE CLASS II; HEXOKINASE; HEXOSE PHOSPHATE; MALIC ACID; PENTOSE PHOSPHATE; TREHALOSE; UNCLASSIFIED DRUG; XYLULOSE 5 PHOSPHATE;

2 KETO 3 DEOXYGLUCONATE KINASE GENE; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; DNA FINGERPRINTING; ENTNER DOUDOROFF PATHWAY; ENZYMATIC DEGRADATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; GENE DELETION; GENE DISRUPTION; GENE LOCATION; GLUCONEOGENESIS; GLUCOSE METABOLISM; GLYCOLYSIS; IN VIVO STUDY; NON PHOSPHORYLATING GAP DEHYDROGENASE GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TRANSPORT; SULFOLOBUS SOLFATARICUS; TRANSCRIPTION INITIATION SITE;

ARCHAEAL PROTEINS; CLONING, MOLECULAR; GENE DELETION; GLYCERIC ACIDS; GLYCOLYSIS; HEXOKINASE; KINETICS; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); SULFOLOBUS SOLFATARICUS;

ARCHAEA; CRENARCHAEOTA; SULFOLOBUS SOLFATARICUS;

EID: 84874108553     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12106     Document Type: Article

References (35)

1. Woese CR, &, Fox GE, (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74, 5088-5090.
2. Verhees CH, Kengen SWM, Tuininga JE, Schut GJ, Adams MWW, De Vos WM, &, Van Der Oost J, (2004) Erratum: The unique features of glycolytic pathways in Archaea (Biochemical Journal (2003) 375 (231-246)). Biochem J 377, 819-822.
3. Siebers B, &, Schönheit P, (2005) Unusual pathways and enzymes of central carbohydrate metabolism in Archaea. Curr Opin Microbiol 8, 695-705.
4. Sato T, &, Atomi H, (2011) Novel metabolic pathways in Archaea. Curr Opin Microbiol 14, 307-314.
5. 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.
6. De Rosa M, Gambacorta A, Nicolaus B, Giardina P, Poerio E, &, Buonocore V, (1984) Glucose metabolism in the extreme thermoacidophilic archaebacterium Sulfolobus solfataricus. Biochem J 224, 407-414.
7. 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.
8. 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.
9. 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.
10. Lamble HJ, Milburn CC, Taylor GL, Hough DW, &, Danson MJ, (2004) Gluconate dehydratase from the promiscuous Entner-Doudoroff pathway in Sulfolobus solfataricus. FEBS Lett 576, 133-136.
11. Kim S, &, Lee SB, (2005) Identification and characterization of Sulfolobus solfataricus D-gluconate dehydratase: a key enzyme in the non-phosphorylated Entner-Doudoroff pathway. Biochem J 387, 271-280.
12. 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.
13. 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.
14. 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.
15. Kardinahl S, Schmidt CL, Hansen T, Anemüller S, Petersen A, &, Schäfer G, (1999) The strict molybdate-dependence of glucose-degradation by the thermoacidophile Sulfolobus acidocaldarius reveals the first crenarchaeotic molybdenum containing enzyme-an aldehyde oxidoreductase. Eur J Biochem 260, 540-548.
16. Kehrer D, Ahmed H, Brinkmann H, &, Siebers B, (2007) Glycerate kinase of the hyperthermophilic archaeon Thermoproteus tenax: new insights into the phylogenetic distribution and physiological role of members of the three different glycerate kinase classes. BMC Genomics 8, 301.
17. Reher M, Bott M, &, Schönheit P, (2006) Characterization of glycerate kinase (2-phosphoglycerate forming), a key enzyme of the nonphosphorylative Entner-Doudoroff pathway, from the thermoacidophilic euryarchaeon Picrophilus torridus. FEMS Microbiol Lett 259, 113-119.
18. Noh M, Jung JH, &, Lee SB, (2006) Purification and characterization of glycerate kinase from the thermoacidophilic archaeon Thermoplasma acidophilum: an enzyme belonging to the second glycerate kinase family. Biotechnol Bioprocess Engineer 11, 344-350.
19. Liu B, Hong Y, Wu L, Li Z, Ni J, Sheng D, &, Shen Y, (2007) A unique highly thermostable 2-phosphoglycerate forming glycerate kinase from the hyperthermophilic archaeon Pyrococcus horikoshii: gene cloning, expression and characterization. Extremophiles 11, 733-739.
20. Liu B, Wu L, Liu T, Hong Y, Shen Y, &, Ni J, (2009) A MOFRL family glycerate kinase from the thermophilic crenarchaeon, Sulfolobus tokodaii, with unique enzymatic properties. Biotechnol Lett 31, 1937-1941.
21. Yang C, Rodionov DA, Rodionova IA, Li X, &, Osterman AL, (2008) Glycerate 2-kinase of Thermotoga maritima and genomic reconstruction of related metabolic pathways. J Bacteriol 190, 1773-1782.
22. Potter JA, Kerou M, Lamble HJ, Bull SD, Hough DW, Danson MJ, &, Taylor GL, (2008) The structure of Sulfolobus solfataricus 2-keto-3- deoxygluconate kinase. Acta Crystallogr Biol Crystallogr 64, 1283-1287.
23. Wagner M, Berkner S, Ajon M, Driessen AJM, Lipps G, &, Albers SV, (2009) Expanding and understanding the genetic toolbox of the hyperthermophilic genus Sulfolobus. Biochem Soc Trans 37, 97-101.
24. Albers SV, &, Driessen AJM, (2008) Conditions for gene disruption by homologous recombination of exogenous DNA into the Sulfolobus solfataricus genome. Archaea 2, 145-149.
25. Schelert J, Dixit V, Hoang V, Simbahan J, Drozda M, &, Blum P, (2004) Occurrence and characterization of mercury resistance in the hyperthermophilic Archaeon Sulfolobus solfataricus by use of gene disruption. J Bacteriol 186, 427-437.
26. Zaparty M, Esser D, Gertig S, Haferkamp P, Kouril T, Manica A, Pham TK, Reimann J, Schreiber K, Sierocinski P, et al,. (2009) 'Hot standards' for the thermoacidophilic archaeon Sulfolobus solfataricus. Extremophiles 14, 119-142.
27. Nishimasu H, Fushinobu S, Shoun H, &, Wakagi T, (2006) Identification and characterization of an ATP-dependent hexokinase with broad substrate specificity from the hyperthermophilic archaeon Sulfolobus tokodaii. J Bacteriol 188, 2014-2019.
28. Nishimasu H, Fushinobu S, Shoun H, &, Wakagi T, (2007) Crystal structures of an ATP-dependent hexokinase with broad substrate specificity from the hyperthermophilic archaeon Sulfolobus tokodaii. J Biol Chem 282, 9923-9931.
29. Ahmed H, Tjaden B, Hensel R, &, Siebers B, (2004) Embden-Meyerhof-Parnas and Entner-Doudoroff pathways in Thermoproteus tenax: metabolic parallelism or specific adaptation? Biochem Soc Trans 32, 303-304.
30. Schwarzenbacher R, McMullan D, Krishna SS, Xu Q, Miller MD, Canaves JM, Elsliger MA, Floyd R, Grzechnik SK, Jaroszewski L, et al,. (2006) Crystal structure of a glycerate kinase (TM1585) from Thermotoga maritima at 2.70 Å resolution reveals a new fold. Proteins Struct Funct Genet 65, 243-248.
31. Albers SV, Szabo Z, &, Driessen AJM, (2003) Archaeal homolog of bacterial type IV prepilin signal peptidases with broad substrate specificity. J Bacteriol 185, 3918-3925.
32. Brock TD, Brock KM, Belly RT, &, Weiss RL, (1972) Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Archiv Mikrobiol 84, 54-68.
33. Hiller K, Hangebrauk J, Jäger C, Spura J, Schreiber K, &, Schomburg D, (2009) MetaboliteDetector: comprehensive analysis tool for targeted and nontargeted GC/MS based metabolome analysis. Anal Chem 81, 3429-3439.
34. Orita I, Sato T, Yurimoto H, Kato N, Atomi H, Imanaka T, &, Sakai Y, (2006) The Ribulose Monophosphate Pathway Substitutes for the Missing Pentose Phosphate Pathway in the Archaeon Thermococcus kodakaraensis. J Bacteriol 188, 4698-4704.
35. Zaparty M, &, Siebers B, (2010) Physiology, Metabolism and Enzymology of Thermoacidophiles. In Extremophiles Handbook (Horikoshi K, Antranikian G, Bull AT, Robb FT & Stetter KO, eds), pp. 602-639. Springer, Tokyo.