Extreme catalysts from low-temperature environments

[en] Cold-loving or psychrophilic organisms are widely distributed in nature as a large part of the earth's surface is at temperatures around 0 degrees C. To maintain metabolic rates and to prosper in cold environments, these extremophilic organisms have developed a vast array of adaptations. One main adaptive strategy developed in order to cope with the reduction of chemical reaction rates induced by low temperatures is the synthesis of cold-adapted or psychrophilic enzymes. These enzymes are characterized by a high catalytic activity at low temperatures associated with a low thermal stability. A study of protein adaptation strategies suggests that the high activity of psychrophilic enzymes could be achieved by the destabilization of the active site, allowing the catalytic center to be more flexible at low temperatures, whereas other protein regions may be destabilized or as rigid as their mesophilic counterparts. Due to these particular properties, psychrophilic enzymes offer a high potential not only for fundamental research but also for biotechnological applications.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Hoyoux, A.

Blaise, Vinciane ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Département des sciences et gestion de l'environnement

Collins, T.

D'Amico, Salvino ; Université de Liège - ULiège > GIGA-Research

Gratia, E.

Huston, A. L.

Marx, J. C.

Sonan, G.

Zeng, Y.

Feller, Georges ; Université de Liège - ULiège > Département des sciences de la vie > Labo de biochimie

Gerday, Charles ; Université de Liège - ULiège > Services généraux (Faculté des sciences) > Relations académiques et scientifiques (Sciences)

Language :

English

Title :

Extreme catalysts from low-temperature environments

Publication date :

November 2004

Journal title :

Journal of Bioscience and Bioengineering

ISSN :

1389-1723

eISSN :

1347-4421

Publisher :

Soc Bioscience Bioengineering Japan, Osaka, Japan

Volume :

Issue :

Pages :

317-330

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 26 January 2010

Statistics

Number of views

57 (0 by ULiège)

Number of downloads

393 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Forster, J.: Ueber einige Eigenschaften leuchtender Bakterien. Centr. Bakteriol. Parasitenk., 2, 337-340 (1887).
Schmidt-Nielsen, S.: Centralbl. Bakteriol. Parasitenkd. Il Abt., 9, 145-147 (1902).
Margesin, R., Feller, G., Gerday, C., and Russell, N.J.: Cold-adapted microorganisms: adaptation strategies and biotechnological potential, p. 871-885. In Bitton, G. (ed.), The encyclopedia of environmental microbiology. Wiley, New York (2002).
Morita, R. Y.: Psychrophilic bacteria. Bacteriol. Rev., 39, 144-167 (1975).
Feller, G., Narinx, E., Arpigny, J.-L., Zekhnini, Z., Swings, J., and Gerday, C.: Temperature dependence of growth, enzyme secretion and activity of psychrophilic Antarctic bacteria. Appl. Microbiol. Biotechnol., 41, 477-479 (1994).
Russell, N. J.: Toward a molecular understanding of cold activity of enzymes from psychrophiles. Extremophiles, 4, 83-90 (2000).
Bowman, J. P., McCammon, S. A., Brown, M. V., Nichols, D. S., and McMeekin, T. A.: Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl. Environ. Microbiol., 63, 3068-3078 (1997).
Margesin, R. and Schinner, F.: Efficiency of indigenous and inoculated cold-adapted soil microorganisms for biodegradation of diesel oil in alpine soils. Appl. Environ. Microbiol., 63, 2660-2664 (1997).
Morita, Y., Nakamura, T., Hasan, Q., Murakami, Y., Yokoyama, K., and Tamiya, E.: Cold-active enzymes from cold-adapted bacteria. J. Am. Oil. Chem. Soc., 74, 441-444 (1997).
Deming, J. W.: Psychrophiles and polar regions. Curr. Opin. Microbiol., 5, 301-309 (2002).
Yayanos, A. A.: Microbiology to 10,500 meters in the deep sea. Annu. Rev. Microbiol., 49, 777-805 (1995).
Ewart, K. V., Lin, Q., and Hew, C. L.: Structure, function and evolution of antifreeze proteins. Cell. Mol. Life Sci., 55, 271-283 (1999).
Russell, N. J. and Hamamoto, T.: Psychrophiles, p. 25-45. In Horikoshi, K. and Grant, D. (ed.), Extremophiles: microbial life in extreme environments. Wiley-Liss, New York (1998).
Ermolenko, D. N. and Makhatadze, G. I.: Bacterial cold-shock proteins. Cell. Mol. Life Sci., 59, 1902-1913 (2002).
Hebraud, M. and Guzzo, J.: The main cold shock protein of Listeria monocytogenes belongs to the family of ferritin-like proteins. FEMS Microbiol. Lett., 190, 29-34 (2000).
Berger, F., Normand, P., and Potier, P.: capA, a cspA-like gene that encodes a cold acclimation protein in the psychrotrophic bacterium Arthrobacter globiformis S155. J. Bacteriol., 179, 5670-5676 (1997).
Michel, V., Lehoux, I., Depret, G., Anglade, P., Labadie, J., and Hebraud, M.: The cold shock response of the psychrotrophic bacterium Pseudomonas fragi involves four low-molecular-mass nucleic acid-binding proteins. J. Bacteriol., 179, 7331-7342 (1997).
Saunders, N. F., Thomas, T., Curmi, P. M., Mattick, J. S., Kuczek, E., Slade, R., Davis, J., Franzmann, P. D., Boone, D., Rusterholtz, K., and 15 other authors: Mechanisms of thermal adaptation revealed from the genomes of the Antarctic Archaea Methanogenium frigidum and Methanococcoides burtonii. Genome Res., 13, 1580-1588 (2003).
Detrich, H. W., 3rd: Molecular adaptation of microtubules and microtubules motors from Antarctic fish, p. 139-149. In di Prisco, G., Pisano, E., and Clarke, A. (ed.), Fishes of Antarctica. A biological review. Springer-Verlag, Milano (1998).
Detrich, H. W., 3rd, Parker, S. K., Williams, R. C., Jr., Nogales, E., and Downing, K. H.: Cold adaptation of microtubule assembly and dynamics. Structural interpretation of primary sequence changes present in the α- and β-tubulins of Antarctic fishes. J. Biol. Chem., 275, 37038-37047 (2000).
Willem, S., Srahna, M., Devos, N., Gerday, C., Loppes, R., and Matagne, R. F.: Protein adaptation to low temperatures: a comparative study of α-tubulin sequences in mesophilic and psychrophilic algae. Extremophiles, 3, 221-226 (1999).
Smalas, A. O., Leiros, H. K., Os, V., and Willassen, N. P.: Cold adapted enzymes. Biotechnol. Annu. Rev., 6, 1-57 (2000).
Gianese, G., Bossa, E, and Pascarella, S.: Comparative structural analysis of psychrophilic and meso- and thermophilic enzymes. Proteins, 47, 236-249 (2002).
D'Amico, S., Gerday, C., and Feller, G.: Structural determinants of cold adaptation and stability in a large protein. J. Biol. Chem., 276, 25791-25796 (2001).
D'Amico, S., Gerday, C., and Feller, G.: Temperature adaptation of proteins: engineering mesophilic-like activity and stability in a cold-adapted α-amylase. J. Mol. Biol., 332, 981-988 (2003).
Lonhienne, T., Zoidakis, J., Vorgias, C. E., Feller, G., Gerday, C., and Bouriotis, V.: Modular structure, local flexibility and cold-activity of a novel chitobiase from a psychrophilic Antarctic bacterium. J. Mol. Biol., 310, 291-297 (2001).
Feller, G., D'Amico, S., Benotmane, A. M., Joly, E, Van Beeumen, J., and Gerday, C.: Characterization of the C-terminal propeptide involved in bacterial wall spanning of α-amylase from the psychrophile Alteromonas haloplanctis. J. Biol. Chem., 273, 12109-12115 (1998).
Bentahir, M., Feller, G., Aittaleb, M., Lamotte-Brasseur, J., Himri, T., Chessa, J. P., and Gerday, C.: Structural, kinetic, and calorimetric characterization of the cold-active phosphoglycerate kinase from the antarctic Pseudomonas sp. TAC1118. J. Biol. Chem., 275, 11147-11153 (2000).
Leiros, I., Moe, E., Lanes, O., Smalas, A. O., and Willassen, N. P.: The structure of uracil-DNA glycosylase from Atlantic cod (Gadus morhua) reveals cold-adaptation features. Acta Crystallogr. D Biol. Crystallogr., 59, 1357-1365 (2003).
Aghajari, N., Van Petegem, E, Villeret, V., Chessa, J. P., Gerday, C., Haser, R., and Van Beeumen, J.: Crystal structures of a psychrophilic metalloprotease reveal new insights into catalysis by cold-adapted proteases. Proteins, 50, 636-647 (2003).
Van Petegem, F., Collins, T., Meuwis, M. A., Gerday, C., Feller, G., and Van Beeumen, J.: The structure of a cold-adapted family 8 xylanase at 1.3 Å resolution, structural adaptations to cold and investigation of the active site. J. Biol. Chem., 278, 7531-7539 (2003).
Russell, R. J., Gerike, U., Danson, M. J., Hough, D. W., and Taylor, G. L.: Structural adaptations of the cold-active citrate synthase from an Antarctic bacterium. Structure, 6, 351-361 (1998).
Aghajari, N., Feller, G., Gerday, C., and Haser, R.: Crystal structures of the psychrophilic α-amylase from Alteromonas haloplanctis in its native form and complexed with an inhibitor. Protein Sci., 7, 564-572 (1998).
Alvarez, M., Zeelen, J. P., Mainfroid, V., Rentier-Delrue, F., Martial, J. A., Wyns, L., Wierenga, R. K., and Maes, D.: Triose-phosphate isomerase (TIM) of the psychrophilic bacterium Vibrio marinus. Kinetic and structural properties. J. Biol. Chem., 273, 2199-2206 (1998).
Kim, S. Y., Hwang, K. Y., Kim, S. H., Sung, H. C., Han, Y.S., and Cho, Y.J.: Structural basis for cold adaptation. Sequence, biochemical properties, and crystal structure of malate dehydrogenase from a psychrophile Aquaspirillium arcticum. J. Biol. Chem., 274, 11761-11767 (1999).
de Backer, M., McSweeney, S., Rasmussen, H. B., Riise, B. W., Lindley, P., and Hough, E.: The 1.9 Å crystal structure of heat-labile shrimp alkaline phosphatase. J. Mol. Biol., 318, 1265-1274 (2002).
Smalas, A. O., Heimstad, E. S., Hordvik, A., Willassen, N. P., and Male, R.: Cold adaption of enzymes: structural comparison between salmon and bovine trypsins. Proteins, 20, 149-166 (1994).
Toyota, E., Ng, K. K., Kuninaga, S., Sekizaki, H., Itoh, K., Tanizawa, K., and James, M. N.: Crystal structure and nucleotide sequence of an anionic trypsin from chum salmon (Oncorhynchus keta) in comparison with Atlantic salmon (Salmo salar) and bovine trypsin. J. Mol. Biol., 324, 391-397 (2002).
Berglund, G. I., Willassen, N. P., Horvik, A., and Smalas, A. O.: Structure of native pancreatic elastase from North Atlantic salmon at 1.61 Å resolution. Acta Cryst. D Biol. Crystallogr., D51, 925-937 (1995).
Karlsen, S., Hough, E., and Olsen, R. L.: Structure and proposed amino-acid sequence of a pepsin from atlantic cod (Gadus morhua). Acta Crystallogr. D Biol. Crystallogr., 54, 32-46 (1998).
Matsuura, A., Yao, M., Aizawa, T., Koganesawa, N., Masaki, K., Miyazawa, M., Demura, M., Tanaka, I., Kawano, K., and Nitta, K.: Structural analysis of an insect lysozyme exhibiting catalytic efficiency at low temperatures. Biochemistry, 41, 12086-12092 (2002).
Aghajari, N., Feller, G., Gerday, C., and Haser, R.: Struc-tures of the psychrophilic Alteromonas haloplanctis α-amylase give insights into cold adaptation at a molecular level. Structure, 6, 1503-1516 (1998).
Violot, S., Haser, R., Sonan, G., Georlette, D., Feller, G., and Aghajari, N.: Expression, purification, crystallization and preliminary X-ray crystallographic studies of a psychrophilic cellulase from Pseudoalteromonas haloplanktis. Acta Crystallogr. D Biol. Crystallogr., 59, 1256-1258 (2003).
Tsuruta, H., Mikami, B., Yamamoto, C., and Aizono, Y.: Crystallization and preliminary X-ray studies of cold-active protein-tyrosine phosphatase of Shewanella sp. Acta Crystallogr. D Biol. Crystallogr., 58, 1465-1466 (2002).
Mandelman, D., Bentahir, M., Feller, G., Gerday, C., and Haser, R.: Crystallization and preliminary X-ray analysis of a bacterial psychrophilic enzyme, phosphoglycerate kinase. Acta Crystallogr. D Biol. Crystallogr., 57, 1666-1668 (2001).
Bell, G. S., Russell, R. J., Connaris, H., Hough, D. W., Danson, M. J., and Taylor, G. L.: Stepwise adaptations of citrate synthase to survival at life's extremes. From psychrophile to hyperthermophile. Eur. J. Biochem., 269, 6250-6260 (2002).
Bae, E. and Phillips, G. N., Jr.: Structures and analysis of highly homologous psychrophilic, mesophilic, and thermophilic adenylate kinases. J. Biol. Chem., 279, 28202-28208 (2004).
Georlette, D., Damien, B., Blaise, V., Depiereux, E., Uversky, V. N., Gerday, C., and Feller, G.: Structural and functional adaptations to extreme temperatures in psychrophilic, mesophilic, and thermophilic DNA ligases. J. Biol. Chem., 278, 37015-37023 (2003).
Aghajari, N., Roth, M., and Haser, R.: Crystallographic evidence of a transglycosylation reaction: ternary complexes of a psychrophilic α-amylase. Biochemistry, 41, 4273-4280 (2002).
Vieille, C. and Zeikus, G. J.: Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol. Mol. Biol. Rev., 65, 1-43 (2001).
Dams, T., Auerbach, G., Bader, G., Jacob, U., Ploom, T., Huber, R., and Jaenicke, R.: The crystal structure of dihydrofolate reductase from Thermotoga maritima: molecular features of thermostability. J. Mol. Biol., 297, 659-672 (2000).
Xu, Y., Feller, G., Gerday, C., and Glansdorff, N.: Moritella cold-active dihydrofolate reductase: are there natural limits to optimization of catalytic efficiency at low temperature? J. Bacteriol., 185, 5519-5526 (2003).
Villeret, V., Clantin, B., Tricot, C., Legrain, C., Roovers, M., Stalon, V., Glansdorff, N., and Van Beeumen, J.: The crystal structure of Pyrococcusfuriosus ornithine carbamoyl-transferase reveals a key role for oligomerization in enzyme stability at extremely high temperatures. Proc. Natl. Acad. Sci. USA, 95, 2801-2806 (1998).
Neet, K. E. and Timm, D. E.: Conformational stability of dimeric proteins: quantitative studies by equilibrium denaturation. Protein Sci., 3, 2167-2174 (1994).
Kirino, H., Aoki, M., Aoshima, M., Hayashi, Y., Ohba, M., Yamagishi, A., Wakagi, T., and Oshima, T.: Hydrophobic interaction at the subunit interface contributes to the thermostability of 3-isopropylmalate dehydrogenase from an extreme thermophile, Thermus thermophilus. Eur. J. Biochem., 220, 275-281 (1994).
Moriyama, H., Onodera, K., Sakurai, M., Tanaka, N., Kirino-Kagawa, H., Oshima, T., and Katsube, Y.: The crystal structures of mutated 3-isopropylmalate dehydrogenase from Thermus thermophilus HB8 and their relationship to the thermostability of the enzyme. J. Biochem. (Tokyo), 117, 408-413 (1995).
Rentier-Delrue, F., Mande, S. C., Moyens, S., Terpstra, P., Mainfroid, V., Goraj, K., Lion, M., Hol, W. G., and Martial, J. A.: Cloning and overexpression of the triosephosphate isomerase genes from psychrophilic and thermophilic bacteria. Structural comparison of the predicted protein sequences. J. Mol. Biol., 229, 85-93 (1993).
Kumar, S. and Nussinov, R.: Different roles of electrostatics in heat and in cold: adaptation by citrate synthase. Chembiochem, 5, 280-290 (2004).
Hoyoux, A., Jennes, I., Dubois, P., Genicot, S., Dubail, F., Francois, J. M., Baise, E., Feller, G., and Gerday, C.: Cold-adapted β-galactosidase from the Antarctic psychrophile Pseudoalteromonas haloplanktis. Appl. Environ. Microbiol., 67, 1529-1535 (2001).
Juers, D. W., Jacobson, R. W., Wigley, D., Zhang, X. J., Huber, R. E., Tronrud, D. E., and Matthews, B. W.: High resolution refinement of β-galactosidase in a new crystal form reveals multiple metal-binding sites and provides a structural basis for α-complementation. Protein Sci., 9, 1685-1699 (2000).
Lonhienne, T., Gerday, C., and Feller, G.: Psychrophilic enzymes: revisiting the thermodynamic parameters of activation may explain local flexibility. Biochim. Biophys. Acta, 1543, 1-10 (2000).
Kramers, H. A.: Brownian motion in field of force and the diffusion model of chemical reactions. Physica, 7, 284-304 (1940).
Fields, P. A. and Somero, G. N.: Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A(4) orthologs of Antarctic notothenioid fishes. Proc. Natl. Acad. Sci. USA, 95, 11476-11481 (1998).
D'Amico, S., Marx, J. C., Gerday, C., and Feller, G.: Activity-stability relationships in extremophilic enzymes. J. Biol. Chem., 278, 7891-7896 (2003).
Collins, T., Meuwis, M.A., Gerday, C., and Feller, G.: Activity, stability and flexibility in glycosidases adapted to extreme thermal environments. J. Mol. Biol., 328, 419-428 (2003).
Cavicchioli, R., Siddiqui, K. S., Andrews, D., and Sowers, K. R.: Low-temperature extremophiles and their applications. Curr. Opin. Biotechnol., 13, 253-261 (2002).
Xu, Y., Feller, G., Gerday, C., and Glansdorff, N.: Metabolic enzymes from psychrophilic bacteria: challenge of adaptation to low temperatures in ornithine carbamoyltransferase from Moritella abyssi. J. Bacteriol., 185, 2161-2168 (2003).
Coker, J. A., Sheridan, P. P., Loveland-Curtze, J., Gutshall, K. R., Auman, A. J., and Brenchley, J. E.: Biochemical characterization of a β-galactosidase with a low temperature optimum obtained from an Antarctic arthrobacter isolate. J. Bacteriol., 185, 5473-5482 (2003).
Kumar, S., Tsai, C. J., and Nussinov, R.: Maximal stabilities of reversible two-state proteins. Biochemistry, 41, 5359-5374 (2002).
Feller, G., d'Amico, D., and Gerday, C.: Thermodynamic stability of a cold-active α-amylase from the Antarctic bacterium Alteromonas haloplanctis. Biochemistry, 38, 4613-4619 (1999).
Becktel, W. J. and Schellman, J. A.: Protein stability curves. Biopolymers, 26, 1859-1877 (1987).
Makhatadze, G. I. and Privalov, P. L.: Energetics of protein structure. Adv. Protein Chem., 47, 307-425 (1995).
Tsai, C. J., Ma, B., and Nussinov, R.: Folding and binding cascades: shifts in energy landscapes. Proc. Natl. Acad. Sci. USA, 96, 9970-9972 (1999).
Kumar, S., Ma, B., Tsai, C. J., Sinha, N., and Nussinov, R.: Folding and binding cascades: dynamic landscapes and population shifts. Protein Sci., 9, 10-19 (2000).
Ma, B., Kumar, S., Tsai, C. J., and Nussinov, R.: Folding funnels and binding mechanisms. Protein Eng., 12, 713-720 (1999).
Wintrode, P. L. and Arnold, F. H.: Temperature adaptation of enzymes: lessons from laboratory evolution. Adv. Protein Chem., 55, 161-225 (2000).
Cherry, J. R., Lamsa, M. H., Schneider, P., Vind, J., Svendsen, A., Jones, A., and Pedersen, A. H.: Directed evolution of a fungal peroxidase. Nat. Biotechnol., 17, 379-384 (1999).
Giver, L., Gershenson, A., Freskgard, P. O., and Arnold, F. H.: Directed evolution of a thermostable esterase. Proc. Natl. Acad. Sci. USA, 95, 12809-12813 (1998).
Miyazaki, K., Wintrode, P. L., Grayling, R. A., Rubingh, D. N., and Arnold, F. H.: Directed evolution study of temperature adaptation in a psychrophilic enzyme. J. Mol. Biol., 297, 1015-1026 (2000).
Roovers, M., Sanchez, R., Legrain, C., and Glansdorff, N.: Experimental evolution of enzyme temperature activity profile: selection in vivo and characterization of low-temperature-adapted mutants of Pyrococcusfuriosus ornithine carbamoyltransferase. J. Bacteriol., 183, 1101-1105 (2001).
Taguchi, S., Ozaki, A., and Momose, H.: Engineering of a cold-adapted protease by sequential random mutagenesis and a screening system. Appl. Environ. Microbiol., 64, 492-495 (1998).
Lebbink, J. H., Kaper, T., Bron, P., van der Oost, J., and de Vos, W. M.: Improving low-temperature catalysis in the hyperthermostable Pyrococcusfuriosus β-glucosidase CelB by directed evolution. Biochemistry, 39, 3656-3665 (2000).
Merz, A., Yee, M. C., Szadkowski, H., Pappenberger, G., Crameri, A., Stemmer, W. P., Yanofsky, C., and Kirschner, K.: Improving the catalytic activity of a thermophilic enzyme at low temperatures. Biochemistry, 39, 880-889 (2000).
Yasugi, M., Amino, M., Suzuki, T., Oshima, T., and Yamagishi, A.: Cold adaptation of the thermophilic enzyme 3-isopropylmalate dehydrogenase. J. Biochem. (Tokyo), 129, 477-484 (2001).
Lonn, A., Gardonyi, M., van Zyl, W., Hahn-Hagerdal, B., and Otero, R. C.: Cold adaptation of xylose isomerase from Thermus thermophilus through random PCR mutagenesis. Gene cloning and protein characterization. Eur. J. Biochem., 269, 157-163 (2002).
Sterner, R., Kleemann, G. R., Szadkowski, H., Lustig, A., Hennig, M., and Kirschner, K.: Phosphoribosyl anthranilate isomerase from Thermotoga maritima is an extremely stable and active homodimer. Protein Sci., 5, 2000-2008 (1996).
Fields, P. A.: Protein function at thermal extremes: balancing stability and flexibility. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 129, 417-431 (2001).
Hochachka, P. W. and Somero, G. N.: Temperature adaptation, p. 355-449. In Hochacka, P. W. and Somero, G. N. (ed.), Biochemical adaptations. Princeton University Press, Princeton (1984).
Tehei, M., Franzetti, B., Madern, D., Ginzburg, M., Ginzburg, B. Z., Giudici-Orticoni, M. T., Bruschi, M., and Zaccai, G.: Adaptation to extreme environments: macromolecular dynamics in bacteria compared in vivo by neutron scattering. EMBO Rep., 5, 66-70 (2004).
Zaccai, G.: How soft is a protein? A protein dynamics force constant measured by neutron scattering. Science, 288, 1604-1607 (2000).
Kohen, A., Cannio, R., Bartolucci, S., and Klinman, J. P.: Enzyme dynamics and hydrogen tunnelling in a thermophilic alcohol dehydrogenase. Nature, 399, 496-499 (1999).
Zavodszky, P., Kardos, J., Svingor, A., and Petsko, G. A.: Adjustment of conformational flexibility is a key event in the thermal adaptation of proteins. Proc. Natl. Acad. Sci. USA, 95, 7406-7411 (1998).
Wrba, A., Schweiger, A., Schultes, V., Jaenicke, R., and Zavodsky, P.: Extremely thermostable D-glyceraldehyde-3-phosphate dehydrogenase from the eubacterium Thermotoga maritima. Biochemistry, 29, 7584-7592 (1990).
Svingor, A., Kardos, J., Hajdu, I., Nemeth, A., and Zavodszky, P.: A better enzyme to cope with cold comparative flexibility studies on psychrotrophic, mesophilic, and thermophilic ipmdhs. J. Biol. Chem., 276, 28121-28125 (2001).
Fitter, J., Herrmann, R., Dencher, N. A., Blume, A., and Hauss, T.: Activity and stability of a thermostable α-amylase compared to its mesophilic homologue: mechanisms of thermal adaptation. Biochemistry, 40, 10723-10731 (2001).
Ichikawa, J. K. and Clarke, S.: A highly active protein repair enzyme from an extreme thermophile: the L-isoaspartyl methyltransferase from Thermotoga maritima. Arch. Biochem. Biophys., 358, 222-231 (1998).
Merz, A., Knochel, T., Jansonius, J. N., and Kirschner, K.: The hyperthermostable indoleglycerol phosphate synthase from Thermotoga maritima is destabilized by mutational disruption of two solvent-exposed salt bridges. J. Mol. Biol., 288, 753-763 (1999).
Aguilar, C. F., Sanderson, I., Moracci, M., Ciaramella, M., Nucci, R., Rossi, M., and Pearl, L. H.: Crystal structure of the β-glycosidase from the hyperthermophilic archeon Sulfolobus solfataricus: resilience as a key factor in thermostability. J. Mol. Biol., 271, 789-802 (1997).
Jaenicke, R.: Do ultrastable proteins from hyperthermophiles have high or low conformational rigidity? Proc. Natl. Acad. Sci. USA, 97, 2962-2964 (2000).
Tehei, M., Madern, D., Pfister, C., and Zaccai, G.: Fast dynamics of halophilic malate dehydrogenase and BSA measured by neutron scattering under various solvent conditions influencing protein stability. Proc. Natl. Acad. Sci. USA, 98, 14356-14361 (2001).
Hernandez, G., Jenney, F.E., Jr., Adams, M.W., and LeMaster, D. M.: Millisecond time scale conformational flexibility in a hyperthermophile protein at ambient temperature. Proc. Natl. Acad. Sci. USA, 97, 3166-3170 (2000).
Margesin, R., Feller, G., Gerday, C., and Russell, N.: Cold-adapted microorganisms: adaptation strategies and biotechnological potential, p. 871-885. In Bitton, G. (ed.), The encyclopedia of environmental microbiology. John Wiley & Sons, New York (2002).
Feller, G., Le Bussy, O., and Gerday, C.: Expression of psychrophilic genes in mesophilic hosts: assessment of the folding state of a recombinant α-amylase. Appl. Environ. Microbiol., 64, 1163-1165 (1998).
Tutino, M. L., Duilio, A., Parrilli, R., Remaut, E., Sannia, G., and Marino, G.: A novel replication element from an Antarctic plasmid as a tool for the expression of proteins at low temperature. Extremophiles, 5, 257-264 (2001).
Gerday, C., Aittaleb, M., Bentahir, M., Chessa, J. P., Claverie, P., Collins, T., D'Amico, S., Dumont, J., Garsoux, G., Georlette, D., and 4 other authors: Cold-adapted enzymes: from fundamentals to biotechnology. Trends Biotechnol., 18, 103-107 (2000).
Feller, G., Lonhienne, T., Deroanne, C., Libioulle, C., Van Beeumen, J., and Gerday, C.: Purification, characterization, and nucleotide sequence of the thermolabile α-amylase from the antarctic psychrotroph Alteromonas haloplanctis A23. J. Biol. Chem., 267, 5217-5221 (1992).