Hyperthermophilic enzymes - Stability, activity and implementation strategies for high temperature applications

FEBS Journal

Volumn 274, Issue 16, 2007, Pages 4044-4056

  Unsworth, Larry D ^b   Van Der Oost, John ^c   Koutsopoulos, Sotirios ^a  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Adsorption; Covalent bonding; Encapsulation; Genomic and proteomic considerations; Hyperthermostable enzymes; Ion pairs; Protein immobilization; Structural features

Indexed keywords

ENZYME; PROTEOME; TRANSCRIPTOME;

ADSORPTION; BIOTECHNOLOGY; COVALENT BOND; ENCAPSULATION; ENZYME ACTIVITY; ENZYME IMMOBILIZATION; ENZYME STABILITY; GENETIC TRANSCRIPTION; GENOMICS; HIGH TEMPERATURE; HYPERTHERMOPHILE; INDUSTRY; LOW TEMPERATURE; MESOPHILE; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; SCREENING; SHORT SURVEY; THERMOPHILE; THERMOSTABILITY;

ENZYME STABILITY; ENZYMES; ENZYMES, IMMOBILIZED; GENOMICS; HEAT; INDUSTRIAL MICROBIOLOGY; PROTEIN ENGINEERING; PROTEOMICS;

EID: 34547747311     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.05954.x     Document Type: Short Survey

References (124)

1. Stetter KO (1996) Hyperthermophilic prokaryotes. FEMS Microbiol Rev 18, 149 158.
2. Woese CR, Kandler O Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains archaea, bacteria, and eucarya. Proc Natl Acad Sci USA 87, 4576 4579.
3. Woese CR (1998) The universal ancestor. Proc Natl Acad Sci USA 95, 6854 6859.
4. Miller SL Lazcano A (1995) The origin of life - did it occur at high temperatures? J Mol Evol 41, 689 692.
5. Forterre P (1996) A hot topic: the origin of hyperthermophiles. Cell 85, 789 792.
6. Brock TD, Brock KM, Belly RT Weiss RL (1972) Sulfolobus: a new genus of sulfur-oxidizing bacteria living in low pH and high temperature. Arch Mikrobiol 84, 54 68.
7. Stetter KO (2006) History of discovery of the first hyperthermophiles. Extremophiles 10, 357 362.
8. Kashefi K Lovley DR (2003) Extending the upper temperature limit for life. Science 301, 934.
9. Koutsopoulos S, van der Oost J Norde W (2005) Temperature dependant structural and functional features of a hyperthermostable enzyme using elastic neutron scattering. Proteins 61, 377 384.
10. Hickey DA Singer GAC (2004) Genomic and proteomic adaptations to growth at high temperature. Genome Biol 5, 117 121.
11. Russell AP Holleman DS (1974) The thermal denaturation of DNA: average length and composition of denatured areas. Nucleic Acids Res 1, 959 978.
12. Musto H, Naya H, Zavala A, Romero H, Alvarez-Valin F Bernardi G (2004) Correlations between genomic GC levels and optimal growth temperatures in prokaryotes. EJB Lett 573, 73 77.
13. Basak S Ghosh TC (2005) On the origin of genomic adaptation at high temperature for prokaryotic organisms. Biochem Biophys Res Commun 330, 629 632.
14. Galtier N Lobry JR (1997) Relationships between genomic GC content, RNA secondary structures and optimal growth temperature in prokaryotes. J Mol Evol 44, 632 636.
15. Wang H-C, Xia X Hickey D (2006) Thermal adaptations of the small subunit ribosomal RNA gene: a comparative study. J Mol Evol 63, 120 125.
16. Grogan DW (1998) Hyperthermophiles and the problem of DNA instability. Mol Microbiol 28, 1043 1049.
17. Daniel RM Cowan DA (2000) Biomolecular stability and life at high temperatures. Cell Mol Life Sci 57, 250 264.
18. Atomi H, Matsumi R Imanaka T (2004) Reverse gyrase is not a prerequisite for hyperthermophilic life. J Bacteriol 186, 4829 4833.
19. Vielle C Zeikus GJ (2001) Hyperthermophilic enzymes: sources, uses and molecular mechanisms for thermostability. Microbiol Mol Biol R 65, 1 43.
20. Chan MK, Mukund S, Kletzin A, Adams MW Rees DC (1995) Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxin oxidoreductase. Science 267, 1463 1469.
21. Salminen T, Teplyakov A, Kankare J, Cooperman BS, Lahti R Goldman A (1996) An unusual route to thermostability disclosed by the comparison of Thermus thermophilus and Escherichia coli inorganic pyrophosphatases. Protein Sci 5, 1014 1025.
22. Lee D-W, Hong Y-H, Choe E-A, Lee S-J, Kim S-B, Lee H-S, Oh J-W, Shin H-H Pyun Y-R (2005) A thermodynamic study of mesophilic, thermophilic and hyperthermophilic 1-arabinose isomerases: The effects of divalent metal ions on protein stability at elevated temperatures. EJB Lett 579, 1261 1266.
23. Britton KL, Baker PJ, Borges KM, Engel PC, Pasquo A, Rice DW, Robb FT, Scandurra R, Stillman TJ Yip KSP (1995) Insights into thermal stability from a comparison of the glutamate-dehydrogenases from Pyrococcus furiosus and Thermococcus litoralis. Eur J Biochem 229, 688 695.
24. Tanaka Y, Tsumoto K, Yasutake Y, Umetsu M, Yao M, Fukada H, Tanaka I Kumagai I (2004) How oligomerization contributes to the thermostability of an Archaeon protein: protein L-isoaspartyl-O-methyltransferase from Sulfolobus tokodaii. J Biol Chem 279, 32957 32967.
25. Karlstrom M, Steen IH, Madern D, Fedoy A-E, Birkeland N-K Ladenstein R (2006) The crystal structure of a hyperthermostable subfamily II isocitrate dehydrogenase from Thermotoga maritima. EJB J 273, 2851 2868.
26. Russell RJM, Ferguson JMC, Haugh DW, Danson MJ Taylor GL (1997) The crystal structure of citrate synthase from the hyperthermophilic bacterium Pyrococcus furiosus at 1.9 ? resolution. Biochemistry 36, 9983 9994.
27. Ramos A, Raven NDH, Sharp RJ, Bartolucci S, Rossi M, Cannio R, Lebbink J, van der Oost J, deVos WM Santos H (1997) Stabilization of enzymes against thermal stress and freeze-drying by mannosylglycerate. Appl Env Microbiol 63, 4020 4025.
28. Eggers DK Valentine JS (2001) Crowding and hydration effects on protein conformation: a study with sol-gel encapsulated proteins. J Mol Biol 314, 911 922.
29. Ellis RJ (2001) Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr Opin Struct Biol 11, 114 119.
30. Tanaka T, Sawano M, Ogasahara K, Sakaguchi Y, Bagautdinov B, Katoh E, Kuroishi C, Shinkai A, Yokoyama S Yutani K (2006) Hyper-thermostability of CutA1 protein, with a denaturation temperature of nearly 150oC. EJB Lett 580, 4224 4230.
31. Elcock AH (1998) The stability of salt bridges at high temperatures: implications for hyperthermophilic proteins. J Mol Biol 284, 489 502.
32. Szilagyi A Zavodszky P (2000) Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Struct Fold Des 8, 493 504.
33. Arnott MA, Michael RA, Thompson CR, Hough DW Danson MJ (2000) Thermostability and thermoactivity of citrate synthases from the thermophilic and hyperthermophilic Archaea, Thermoplasma acidophilum and Pyrococcus furiosus. J Mol Biol 304, 657 668.
34. Tehei M, Madern D, Franzetti B Zaccai G (2005) Neutron scattering reveals the dynamic basis of protein adaptation to extreme temperature. J Biol Chem 280, 40974 40979.
35. Brock TD Freeze H (1969) Thermus aquaticus gen. n. & sp. N., a nonsporulating extreme thermophile. J Bacteriol 98, 289 297.
36. Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239, 487 491.
37. Looger LL, Dwyer MA, Smith JJ Hellinga HW (2003) Computational design of receptor and sensor proteins with novel functions. Nature 423, 185 190.
38. Cherry JR, Lamsa MH, Schneider P, Vind J, Svendsen A, Jones A Pedersen AH (1999) Directed evolution of a fungal peroxidase. Nat Biotechnol 17, 379 384.
39. Lehmann M, Pasamontes L, Lassen SF Wyss M (2000) The consensus concept for thermostability engineering of proteins. Biochim Biophys Acta - Prot Struct Mol Enzymol 1543, 408 415.
40. Crameri A, Whitehorn EA, Tate E Stemmer WPC (1996) Improved green fluorescent protein by molecular evolution using DNA shuffling. Nat Biotechnol 14, 315 319.
41. Bouzas TD, Barros-Velazquez J Villa TG (2006) Industrial applications of hyperthermophilic enzymes: a review. Prot Pept Lett 13, 445 451.
42. Bauer MW, Driskill LE Kelly RM (1998) Glycosyl hydrolases from hyperthermophilic microorganisms. Curr Opin Biotechn 9, 141 145.
43. Haki GD Rakshit SK (2003) Developments in industrially important thermostable enzymes: a review. Biores Technol 89, 17 34.
44. Kim MS, Park JT, Kim YW, Lee HS, Nyawira R, Shin HS, Park CS, Yoo SH, Kim YR, Moon TW et al. (2004) Properties of a novel thermostable glucoamylase from the hyperthermophilic archaeon Sulfolobus solfataricus in relation to starch processing. Appl Environ Microbiol 70, 3933 3940.
45. Piller K, Daniel PM Petach HH (1996) Properties and stabilization of an extracellular alpha-glucosidase from the extremely thermophilic archaebacteria Thermococcus strain AN1: enzyme activity at 130oC. Biochim Biophys Acta - Prot Struct Molec Enzymol 1292, 197 205.
46. Eichler J (2001) Biotechnological uses of archaeal extremozymes. Biotechnol Adv 19, 261 278.
47. Cannio R, Di Prizito N, Rossi M Morana A (2004) A xylan-degrading strain of Sulfolobus solfataricus: isolation and characterization of the xylanase activity. Extremophiles 8, 117 124.
48. Takagi M, Nishioka M, Kakihara H, Kitabayashi M, Inoue H, Kawakami B, Oka M Imanaka T (1997) Characterization of DNA polymerase from Pyrococcus sp. strain KOD1 and its application to PCR. Appl Environ Microbiol 63, 4504 4510.
49. Lundberg KS, Shoemaker DD, Adams MWW, Short JM, Sorge JA Mathur EJ (1991) High-fidelity amplification using a thermostable DNA-polymerase isolated from Pyrococcus-furiosus. Gene 108, 1 6.
50. Matsumoto K, Kazuno Y, Higashimura N, Ohshima T Sakuraba H (2006) Process for Production of Chiral Hydroxyaldehydes. Eur Patent Appication No. 1 734 129. A1.
51. Rao SV, Anderson KW Bachas LG (1998) Oriented immobilization of proteins. Microchim Acta 128, 127 143.
52. Grazu V, Abian O, Mateo C, Batista-Viera F, Fernandez-Lafuente R Guisan JM (2005) Stabilization of enzymes by multipoint immobilization of thiolated proteins on new epoxy-thiol supports. Biotechnol Bioengin 90, 597 605.
53. Eggers DK Valentine JS (2000) Molecular confinement influences protein structure and enhances thermal protein stability. Protein Sci 10, 250 261.
54. Yan M, Ge J, Liu Z Ouyang P (2006) Encapsulation of single enzyme in nanogel with enhanced biocatalytic activity and stability. J Am Chem Soc 128, 11008 11009.
55. Lee C-H, Lang J, Yen C-W, Shih P-C, Lin T-S Mou C-Y (2005) Enhancing stability and oxidation activity of cytochrome c by immobilization in the nanchannels of mesoporous aluminosilicates. J Phys Chem B 109, 12277 12286.
56. Norde W Zoungrana T (1998) Surface-induced changes in the structure and activity of enzymes physically immobilized at solid/liquid interfaces. Biotechnol Appl Biochem 28, 133 143.
57. Norde W (2003) Driving forces for protein adsorption at solid surfaces. In Biopolymers at Interfaces, 2nd edn (Malmsten M, ed.). Marcel Dekker, Inc., New York, NY.
58. Ladero M, Ruiz G, Pessela BCC, Vian A, Santos A Garcia-Ochoa F (2006) Thermal and pH inactivation of an immobilized thermostable beta-glactosidase from Thermus Sp. Strain T2: comparison to the free enzyme. Biochem Eng J 31, 14 24.
59. Simpson HD, Haufler UR Daniel RM (1991) An extremely thermostable xylanase from the thermophilic eubacterium Thermotoga. Biochem J 277, 413 417.
60. Koutsopoulos S, van der Oost J Norde W (2004) Adsorption of an endoglucanase from the hyperthermophilic Pyrococcus furiosus on hydrophobic (polystyrene) and hydrophilic (silica) surfaces increases heat stability. Langmuir 20, 6401 6406.
61. Koutsopoulos S, van der Oost J Norde W (2005) Structural features of an hyperthermostable endo-b-1,3-glucanase in solution and adsorbed on 'invisible' particles. Biophys J 88, 467 474.
62. Unsworth LD, Sheardown H Brash JL (2005) Protein resistance of surfaces prepared by sorption of end-thiolated poly(ethylene glycol) to gold: effect of surface chain density. Langmuir 21, 1036 1041.
63. van Oss CJ (2003) Interfacial Forces in Aqueous Media. Marcel Dekker, Inc, New York, NY.
64. Koutsopoulos S, Tjeerdsma A-M, Lieshout JFT, van der Oost J Norde W (2005) In situ structure and activity studies of an enzyme adsorbed on spectroscopically undetectable particles. Biomacromolecules 6, 1176 1184.
65. Koutsopoulos S, van der Oost J Norde W (2005) Conformational studies of a hyperthermostable enzyme. EJB J 272, 5484 5496.
66. Svendsen A, Clausen IG, Patkar SA, Kim B Thellersen M (1997) Protein engineering of microbial lipases industrial interest. Methods Enzymol 284, 317 340.
67. Brady L, Brzozowski AM, Derwenda ZS, Dodson E, Dodson G, Tolley S, Turkenburg JP, Christiansen L, Huge-Jensen B, Norskov L et al. (1990) A serine protease triad forms the catalytic center of a triacylglycerol lipase. Nature 343, 767 770.
68. Palomo JM, Munoz G, Fernandex-Lorente G, Mateo C, Fernandex-Lafuente R Guisan JM (2002) Interfacial adsorption of lipases on a very hydrophobic support (octadecyl-Sepabeads): immobilization, hyperactivation and stabilization of the open form of lipases. J Mol Catal B Enzym 19-20, 279 286.
69. Wilson L, Palomo JM, Fernandez-Lorente G, Illanes A, Guisan JM Fernandez-Lafuente R (2006) Effect of lipase-lipase interactions in the activity, stability and specificity of a lipase from Alcaligenes sp. Enzyme Microb Tech 39, 259 264.
70. Barrias CC, Martins MCL, Miranda MCS Barbosa MA (2005) Adsorption of a therapeutic enzyme to self-assembled monolayers: effect of surface chemistry and solution pH on the amount and activity of adsorbed enzyme. Biomaterials 26, 2695 2704.
71. Haynes CA Norde W (1994) Globular proteins at solid/liquid interfaces. Colloids Surf B Biointerfaces 2, 517 566.
72. Giacomelli CE Norde W (2001) The adsorption-desorption cycle. Reversibility of the BSA-silica system. J Coll Interf Sci 233, 234 240.
73. Pinheiro HM, Kennedy JF Cabral JMS (1996) Immobilized enzymes and cells. In Interfacial Phenomena and Bioproducts. (Brash JL Wojciechowski PW, eds), pp. 311 350. Marcel Dekker, NewYork, NY.
74. Mateo C, Fernandez-Lorente G, Abian O, Fernandez-Lafuente R Guisan JM (2000) Multifunctional epoxy supports: a new tool to improve the covalent immobilization of proteins. the promotion of physical adsorptions of proteins on the supports before their covalent linkage. Biomacromolecules 1, 739 745.
75. Fernandez-Lafuente R, Cowan DA Wood ANP (1995) Hyperstabilization of a thermophilic esterase by multipoint covalent attachment. Enzyme Microbial Technol 17, 366 372.
76. Saito T, Yoshida Y, Kawashima K, Lin KH, Inagaki H, Maeda S Kobayashi T (1997) Influence of aldehyde groups on the thermostability of an immobilized enzyme on an inorganic support. Mater Sci Eng C - Biomimetic Supramol Syst C5, 149 152.
77. Pierre AC (2004) The sol-gel encapsulation of enzymes. Biocatal Biotransform 22, 145 170.
78. Bolis D, Politou AS, Kelly G, Pastore A Temussi PA (2003) Protein stability in nanocages: a novel approach for influencing protein stability by molecular confinement. J Mol Biol 336, 203 212.
79. Patil AJ, Muthusamy E Mann S (2004) Synthesis and self-assembly of organoclay-wrapped biomolecules. Angew Che Int Ed 43, 4928 4933.
80. Patil AJ, Muthusamy E Mann S (2005) Fabrication of functional protein-organoclay lamellar nanocomposites by biomolecule-induced assembly of exfoliated aminopropyl-functionalized magnesium phyllosilicates. J Mater Chem 15, 3838 3843.
81. Kohda J, Kawanishi H, Suehara K-I, Nakano Y Yano T (2006) Stabilization of free and immobilized enzymes using hyperthermophilic chaperonin. J Biosci Bioeng 101, 131 136.
82. Coradin T, Coupe A Livage J (2003) Intercalation of biomolecules in the MnPS3 layered phase. J Mater Chem 13, 705 707.
83. Brown SH, Costantino HR Kelly RM (1990) Characterization of amylolytic enzyme-activities associated with the hyperthermophilic archaebacterium pyrococcus-furiosus. Appl Environ Microbiol 56, 1985 1991.
84. Jørgensen S, Vorgias CE Antranikian G (1997) Cloning, sequencing, characterization, and expression of an extracellular alpha-amylase from the hyperthermophilic archaeon Pyrococcus furiosus in Escherichia coli and Bacillus subtilis. J Biol Chem 272, 16335 16342.
85. Koch R, Spreinat K, Lemke K Antranikian G (1991) Purification and properties of a hyperthermoactive α-amylase from the archaeobaterium Pyrococcus woesei. Arch Microbiol 155, 572 578.
86. Bragger JM, Daniel RM, Coolbear T Morgan HW (1989) Very stable enzymes from extremely thermophilic archaeabacteria and eubacteria. Appl Microbiol Biotechnol 31, 556 561.
87. Kim JW, Flowers LO, Whiteley M Peeples TL (2001) Biochemical confirmation and characterization of the family-57-like alpha-amylase of Methanococcus jannaschii. Folia Microbiol 46, 467 473.
88. Rüdiger A, Jørgensen PL Antranikian G (1995) Isolation and characterization of a heat stable pullulanase from the hyperthermophilic archeon Pyrococcus woesei after cloning and expression of its gene in Escherichia coli. Appl Environ Microbiol 61, 567 575.
89. Andrade CMMC, Aguiar WB Antranikian G (2001) Physiological aspects involved in production of xylanolytic enzymes by deep-sea hyperthermophilic archaeon Pyrodictium abyssi. Appl Biochem Biotechnol 91, 655 669.
90. Niehaus F, Peters A, Groudieva T Antranikian G (2000) Cloning, expression and biochemical characterisation of a unique thermostable pullulan-hydrolysing enzyme from the hyperthermophilic archaeon Thermococcus aggregans. FEMS Microbiol Lett 190, 223 239.
91. Hansen T, Urbanke C Schönheit P (2004) Bifunctional phopshoglucose/phosphomannose isomerase from the hyperthermophilic archaeon Pyrobaculum aerophilum. Extremophiles 8, 507 512.
92. Brown SH, Sjoholm C Kelly RM (1993) Purification and characterization of a highly thermostable glucose-isomerase produced by the extremely thermophilic eubacterium, Thermotoga-maritima. Biotechnol Bioeng 41, 878 886.
93. Bauer MW, Bylina EJ, Swanson RV Kelly RM (1997) Comparison of a β-glucosidase and a β-mannosidase from the hyperthermophilic archaeon Pyrococcus furiosus. J Biol Chem 271, 23749 23755.
94. Galichet A Belarbi A (1999) Cloning of an α-glucosidase gene from Thermococcus hydrothermalis by functional complementation of a Saccharomyces cerevisiae mal11 mutant strain. EJB Lett 458, 188 192.
95. Léveque E, Janecek S Belarbi HB (2000) Thermophilic archaeal amylolytic enzymes. Enz Microbiol Technol 26, 3 14.
96. Rolfsmeier M, Haseltine C, Bini E, Clark A Blum P (1998) Molecular characterization of the α-glucosidase gene (malA) from the hyperthermophilic archaeon Sulfolobus solfataricus. J Bacteriol 180, 1287 1295.
97. Brown SH Kelly RM (1993) Characterization of amylolytic enzymes, having both α-1,4 and α-1,6 hydrolytic activity, from the thermophilic archaea Pyrococcus furiosus and Thermococcus litoralis. Appl Environ Microbiol 59, 2614 2621.
98. Kengen SWM, Luesink EJ, Stams AJM Zehnder AJB (1993) Purification and characterization of an extremely thermostable β-glucosidase from the hyperthermophilic archaeon Pyrococcus furiosus. Eur J Biochem 213, 305 312.
99. Matsui I, Sakai Y, Matsui E, Kikuchi H, Kawarabayasi Y Honda K (2000) Novel substrate specificity of a membrane-bound beta-glycosidase from the hyperthermophilic archaeon Pyrococcus horikoshii. EJB Lett 467, 195 200.
100. Duffaud GD, McCutchen CM, Leduc P, Parker KN Kelly RM (1997) Purification and characterization of extremely thermostable beta-mannanase, beta-mannosidase, and alpha-galactosidase from the hyperthermophilic eubacterium Thermotoga neapolitana 5068. Appl Environ Microbiol 63, 169 177.
101. Machielsen R van der Oost J (2006) Production and characterization of a thermostable L-threonine dehydrogenase from the hyperthermophilic archaeon. Pyrococcus Furiosus EJB J 273, 2722 2729.
102. Machielsen R, Uria AR, Kengen SWM van der Oost J (2006) Production and characterization of a thermostable alcohol dehydrogenase that belongs to the aldo-keto reductase superfamily. Appl Environ Microbiol 72, 233 238.
103. Cheng TC, Ramakrishnan V Chan SI (1999) Purification and characterization of cobalt-activated carboxypeptidase from the hyperthermophilic Archaeon Pyrococcus furiosus. Protein Sci 8, 2474 2486.
104. Mori K Ishikawa K (2005) New deblocking aminopeptidases from Pyrococcus horikoshii. Biosci Biotech Bioch 69, 1854 1860.
105. Lee HS, Kim YJ, Bae SS, Jeon JH, Lim JK, Jeong BC, Kang SG Lee JH (2006) Cloning, expression, and characterization of aminopeptidase P from the hyperthermophilic archaeon Thermococcus sp strain NA1. Appl Environ Microbiol 72, 1886 1890.
106. Story SV, Shah C, Jenney FE Adams MWW (2005) Characterization of a novel zinc-containing, lysine-specific aminopeptidase from the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 187, 2077 2083.
107. Badr HR, Sims KA Adams MWW (1994) Purification and characterization of a sucrose α-glucohydrolase (invertase) from the hyperthermophilic archaeon Pyrococus furiosus. System Appl Microbiol 17, 1 6.
108. Kengen SWM, Tuininga JE, de Bok FAM, Stams AJM de Vos WM (1995) Purification and characterization of a novel ADP-dependent glucokinase from the hyperthermophilic archaeon Pyrococcus furiosus. J Biol Chem 270, 30453 30457.
109. Cowan DA, Smolenski KA, Daniel RM Morgan HW (1987) An extremely thermostable extracellular proteinase from a strain of the archaebacterium Desulfurococcus growing at 88oC. Biochem J 247, 121 133.
110. Morikawa M, Izawa Y, Rashid N, Hoaki T Imanaka T (1994) Purification and characterization of a thermostable thiol protease from a newly isolated hyperthermophilic Pyrococcus sp. Appl Environ Microbiol 60, 4559 4566.
111. Halio SB, Bauer MW, Mukund S, Adams MWW Kelly RM (1997) Purification and characterization of two functional forms of intracellular protease PfpI from the hyperthermophilic archaeon Pyrococcus furiosus. Appl Environ Microbiol 63, 289 295.
112. Gueguen Y, Voorhorst WGB, van der Oost J de Vos WM (1997) Molecular and biochemical characterization of an endo-b-1,3-glucanase of the hyperthermophilic archaeon Pyrococcus furiosus. J Biol Chem 272, 31258 31264.
113. Johnsen U, Hansen T Schonheit P (2003) Comparative analysis of pyruvate kinases from the hyperthermophilic archaea Archaeoglobus fulgidus, Aeropyrum pernix, and Pyrobaculum aerophilum and the hyperthermophilic bacterium Thermotoga maritima - unusual regulatory properties in hyperthermophilic archaea. J Biol Chem 278, 25417 25427.
114. Cacciapuoti G, Bertoldo C, Brio A, Zappia V Porcelli M (2003) Purification and characterization of 5′-methylthioadenosine phosphorylase from the hyperthermophilic archaeon Pyrococcus furiosus - substrate specificity and primary structure. Extremophiles 7, 159 168.
115. Cacciapuoti G, Porcelli M, Bertoldo C, Derosa M Zappia V (1994) Purification and characterization of extremely thermophilic and thermostable 5′-methylthioadenosine phosphorylase from the archaeon Sulfolobus-solfataricus - purine nucleoside phosphorylase-activity and evidence for intersubunit disulfide bonds. J Biol Chem 269, 24762 24769.
116. Imanaka H, Fukui T, Atomi H Imanaka T (2002) Gene cloning and characterization of fructose-1,6-bisphosphate aldolase from the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1. J Biosci Bioeng 94, 237 243.
117. Buchanan CL, Connaris H, Danson MJ, Reeve CD Hough DW (1999) An extremely thermostable aldolase from Sulfolobus solfataricus with specificity for non-phosphorylated substrates. Biochem J 343, 563 570.
118. Hansen T, Reichstein B, Schmid R Schonheit P (2002) 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.
119. Koga S, Yoshioka I, Sakuraba H, Takahashi M, Sakasegawa S, Shimizu S Ohshima T (2000) Biochemical characterization, cloning, and sequencing of ADP-dependent (AMP-forming) glucokinase from two hyperthermophilic archaea, Pyrococcus furiosus and Thermococcus litoralis. J Biochem 128, 1079 1085.
120. Tachibana Y, Kuramura A, Shirasaka N, Suzuki Y, Yamamoto T, Fujiwara S, Takagi M Imanaka T (1999) Purification and characterization of an extremely thermostable cyclomaltodextrin glucanotransferase from a newly isolated hyperthermophilic archaeon, a Thermococcus sp. Appl Environ Microbiol 65, 1991 1997.
121. Tachibana Y, Fujiwara S, Takagi M Imanaka T (1997) Cloning and expression of the 4-alpha-glucanotransferase gene from the hyperthermophilic archaeon Pyrococcus sp KOD1, and characterization of the enzyme. J Ferment Bioeng 83, 540 548.
122. Ikeda M Clark DS (1998) Molecular cloning of extremely thermostable esterase gene from hyperthermophilic archaeon Pyrococcus furiosus in Escherichia coli. Biotechnol Bioeng 57, 624 629.
123. Sako Y, Croocker PC Ishida Y (1997) An extremely heat-stable extracellular proteinase (aeropyrolysin) from the hyperthermophilic archaeon Aeropyrum pernix K1. EJB Lett 415, 329 334.
124. Story SV, Grunden AM Adams MWW (2001) Characterization of an aminoacylase from the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 183, 4259 4268.