Chapter 13 : Cold-Adapted Enzymes

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Cold-adapted enzymes are produced by microorganisms living at permanently low temperature, which constitutes the major environment on planet Earth and includes deep sea, polar, and mountain regions. This chapter deals with those enzymes that are significantly adapted to low temperatures, that is, displaying a high specific activity at low temperatures. Many enzymes produced by cold-adapted microorganisms have now been fully characterized in terms of their physical, chemical, and kinetic properties but still only 11 structures have been solved by X-ray crystallography: α-amylase, citrate synthase, malate dehydrogenase, triosephosphate isomerase, Ca-Zn protease, xylanase, adenylate kinase, cellulase, subtilisin-like protease, tyrosine phosphatase, and β-galactosidase. The in vitro growth temperature of these psychrophilic microorganisms is very important for enzyme production, especially for extracellular enzymes, since the production is highly dependent on temperature. In another systematic investigation, the production of various extracellular enzymes such as cellulases, pectate lyases, chitinases, and chitobiases by several strains permanently or seasonally exposed to cold temperatures was followed as a function of growth temperature. The structural modifications believed to be involved in cold-adaptation have been examined in some limited cases using site-directed mutagenesis and directed evolution approaches. The two main properties of cold-adaptation enzymes—a high specific activity at low and moderate temperatures and a low thermostability enabling their rapid inactivation in a complex mixture—render these enzymes particularly suitable for various low to moderate temperature biotechnological processes.

Citation: Collins T, D’Amico S, Marx J, Feller G, Gerday C. 2007. Cold-Adapted Enzymes, p 165-179. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch13

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Image of Figure 1.
Figure 1.

Thermodependence of the activity of the cold-adapted cellulase from (◆) compared to that of the mesophilic counterpart from (•).

Citation: Collins T, D’Amico S, Marx J, Feller G, Gerday C. 2007. Cold-Adapted Enzymes, p 165-179. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch13
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Figure 2.

Growth, in rich medium, of the Antarctic strain A23 (left panel) and α-amylase secretion (right panel) at 4°C (◯), 18°C (∎), and 25°C (▲). There is a net inhibition of exoenzyme production and of cell density when the temperature is raised. Adapted from .

Citation: Collins T, D’Amico S, Marx J, Feller G, Gerday C. 2007. Cold-Adapted Enzymes, p 165-179. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch13
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Citation: Collins T, D’Amico S, Marx J, Feller G, Gerday C. 2007. Cold-Adapted Enzymes, p 165-179. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch13
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Citation: Collins T, D’Amico S, Marx J, Feller G, Gerday C. 2007. Cold-Adapted Enzymes, p 165-179. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch13
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Figure 3.

Thermodependence of activity (A, B), upper panel, and unfolding process, as recorded by fluorescence spectroscopy (C), and differential micro-calorimetry (D), of cold-adapted α-amylase (AHA), mesophilic α-amylase from pig pancreas (PPA), thermostable α-amylase from (BAA), family 8 cold-adapted xylanase from Antarctic (pXyl), family 11 mesophilic xylanase from sp. S38(Xyl1), and family 8 thermostable endoglucanase from (CelA). The apparent maximal activities of cold-adapted enzymes, AHA, and pXyl are reached well before any significant structural changes. Adapted from .

Citation: Collins T, D’Amico S, Marx J, Feller G, Gerday C. 2007. Cold-Adapted Enzymes, p 165-179. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch13
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1. Aghajari, N.,, G. Feller,, C. Gerday, and, R. Haser. 1998. Structures of the psychrophilic Alteromonas haloplanktis alpha-amylase give insight into cold adaptation at a molecular level. Structure 6:15031516.
2. Aghajari, N.,, F. Van Petegem,, V. Villeret,, J.-P. Chessa,, C. Gerday,, R. Haser, and, J. Van Beeumen. 2003. Crystal structure of a psychrophilic metalloprotease reveals new insights into catalysis by cold-adapted proteases. Proteins: Struct. Funct. Genet. 50:636647.
3. Aguilar, C. F.,, I. Sanderson,, M. Moracci,, M. Ciaramella,, R. Nucci,, M. Rossi, and, L. H. Pearl. 1997. Crystal structure of the β-glycosidase from the hyperthermophilic archaeon Sulfolobus solfataricus: resilience as a key factor in thermostability. J. Mol. Biol. 271:789802.
4. Alvarez, M.,, J.-P. Zeelen,, V. Mainfroid,, F. Rentier-Delrue,, J. Martial, and, L. Wyns. 1998. Triosephosphate isomerase(TIM) of the psychrophilic bacterium Vibrio marinus. Kinetic and structural properties. J. Biol. Chem. 273:21992206.
5. Arnorsdottir, J.,, M. M.,, Kristjansson, and R. Ficner. 2005. Crystal structure of a subtilisin-like serine proteinase from a psychrotrophic Vibrio species reveals structural aspects of cold adaptation. FEBS J. 272:832845.
6. Arnosti, C.,, and B. Jorgensen. 2003. High activity and low temperature optima of extracellular enzymes in Arctic sediments: implication for carbon cycling by heterotrophic microbial communities. Mar. Ecol. Prog. Ser. 249:1524.
7. Arpigny, J.-L.,, J. Lamotte, and, C. Gerday. 1997. Molecular adaptation to cold of an Antarctic bacterial lipase. J. Mol. Catal. B: Enzymatic. 3:2935.
8. Arrhenius, S. 1889. Uber die reaktionsgeschwindigkeit bei der inversion von rohrzucker durch sauren. Z. Physik. Chem. 4:226248.
9. Astwood, A. C.,, and A. C. Wais. 1998. Psychrotrophic bacteria isolated from a constantly warm tropical environment. Curr. Microbiol. 36:148151.
10. Bae, E.,, and G. N. Phillips. 2004. Structures and analysis of highly homologous psychrophilic, mesophilic, and thermophilic adenylate kinases. J. Biol. Chem. 279:2820228208.
11. Bendt, A.,, H. Huller,, U. Kammel,, E. Helmke, and, T. Schweder. 2001. Cloning, expression and characterization of a chitinase gene from the Antarctic psychrotolerant bacterium Vibrio sp.strain Fi:7. Extremophiles. 5:119126.
12. Bentahir, M.,, G. Feller,, M. Aittaleb,, J. Lamotte-Brasseur,, T. Himri,, J.-P. Chessa, and, C. Gerday. 2000. Structural, kinetic, and calorimetric characterization of a cold-active phosphoglycerate kinase from the Antarctic Pseudomonas sp. TACII 18. J. Biol. Chem. 275:1114711153.
13. Birolo, L.,, M. L. Tutino,, B. Fontanella,, C. Gerday,, K. Mainolfi,, S. Pascarella,, G. Sannia,, F. Vinci, and, G. Marino. 2000. Aspar-tate aminotransferase from the Antarctic bacterium Pseudoalteromonas haloplanktis TAC 125. Eur. J. Biochem. 267:27902802.
14. Bransdal, B. O.,, E. S. Heimstad,, I. Sylte, and, A. O. Smalas. 1999. Comparative molecular dynamics of mesophilic and psychrophilic protein homologues studied by 1.2 ns simulations. J. Biomol. Struct. 3:493506.
15. Buchon, L.,, P. Laurent,, A. M. Gounot, and, J. F. Guespin-Michel. 2000. Temperature dependence of extracellular enzymes production by psychrotrophic and psychrophilic bacteria. Biotechnol. Lett. 22:15771581.
16. Cavicchioli, R.,, K. S. Siddiqui,, D. Andrews, and, K. R. Somers. 2002. Low-temperature extremophiles and their applications. Curr. Opin. Biotechnol. 13:253261.
17. Cieslinski, H.,, J. Kur,, A. Bialkowska,, I. Baran,, K. Makowski, and, M. Turkiewicz. 2005. Cloning, expression and purification of a recombinant cold-adapted β-galactosidase from Antarctic bacterium Pseudoalteromonas sp.22B. Prot. Expr. Purif. 39:2734.
18. Collins, C.,, M-A Meuwis,, I. Stals,, M. Claeyssens,, G. Feller, and, C. Gerday. 2002. A novel family & xylanase, functional and physicochemical characterization. J. Biol. Chem. 277:3513335139.
19. Collins, T.,, M.-A. Meuwis,, C. Gerday, and, G. Feller. 2003. Activity, stability and flexibility in glycosidases adapted to extreme thermal environments. J. Mol. Biol. 328:419428.
20. Chessa, J.-P.,, I. Petrescu,, M. Bentahir,, J. Van Beeumen, and, C. Gerday. 2000. Purification, physico-chemical characterization and sequence of the heat labile alkaline metalloprotease isolated from a psychrophilic Pseudomonas species. Biochim. Biophys. Acta. 1479:265274.
21. D’Amico, S.,, P. Claverie,, T. Collins,, D. Georlette,, E. Gratia,, A. Hoyoux,, M.-A. Meuwis,, G. Feller, and, C. Gerday. 2002. Molecular basis of cold adaptation. Philos. Trans. R. Soc. Lond. Series B.: Biol. Sci. 357:917925.
22. D’Amico, S.,, C. Gerday, and, G. Feller. 2003a. Activity-stability relationships in extremophilic enzymes. J. Biol. Chem. 278:78917896.
23. D’Amico, S.,, C. Gerday, and, G. Feller. 2003b. Temperature adaptation of proteins: engineering mesophilic-like activity and stability in a cold-adapted α-amylase. J. Mol. Biol. 332:981988.
24. Daniel, R. M.,, M. J. Danson, and, R. Eisenthal. 2001. The temperature optima of enzymes: a new perspective on an old phenomenon. Trends Biochem. Sci. 26:223225.
25. Davail, S.,, G. Feller,, E. Narinx, and, C. Gerday. 1994. Cold adaptation of proteins. Purification, characterization, and sequence of the heat–labile subtilisin from the Antarctic psychrophile Bacillus TA41.1994. J. Biol. Chem. 269:1744817453.
26. De Backer, M.,, S. McSweeney,, H. B. Rasmussen,, B. W. Riise,, P. Lindley, and, E. Hough. 2002. The 1.9A crystal structure of heat-labile shrimp alkaline phosphatase. J. Mol. Biol. 318:12651274.
27. Demchenko, A. P.,, O. I. Rusyn, and, E. A. Saburova. 1989. Kinetics of the lactate dehydrogenase reaction in high-viscosity media. Biochim. Biophys. Acta. 998:196203.
28. Deming, J. W. 2002. Psychrophiles and polar regions. Curr. Opin. Microbiol. 5:301309.
29. Demot, R.,, and H. Verachtert. 1987. Purification and characterization of extracellular α-amylase and glucosamylase from the yeast Candida antarctica CBS 6678. Eur. J. Biochem. 4:643654.
30. Evans, M. G.,, and M. Polanyi. 1935. Some applications of the transition state method to the calculation of reaction velocities especially in solution. Trans. Faraday Soc. 31:875894.
31. Eyring, H. 1935. The activated complex in chemical reactions. J. Chem. Phys. 3:107115.
32. Feller, G.,, and C. Gerday. 1997. Psychrophilic enzymes: molecular basis of cold adaptation. CMLS, Cell. Mol. Life Sci. 53:830841.
33. Feller, G.,, and C. Gerday. 2003. Psychrophilic enzymes: hot topics in cold adaptation. Nature Rev. Microbiol. 1:200207.
34. Feller, G.,, E. Narinx,, J.-L. Arpigny,, Z. Zekhnini, and, C. Gerday. 1994. Temperature dependence of growth, enzyme secretion and activity of psychrophilic Antarctic bacteria. Appl. Microbiol. Biotechnol. 41:477479.
35. Feller, G.,, E. Narinx,, J.-L. Arpigny,, M. Aittaleb,, E. Baise,, S. Genicot, and, C. Gerday. 1996. Enzymes from psychrophilic organisms. FEMS Microbiol. Rev. 18:189202.
36. Feller, G.,, D. d’Amico, and, C. Gerday. 1999. Thermodynamic stability of a cold-active α-amylase from the Antarctic bacterium Alteromonas haloplanktis. Biochemistry. 38:46134619.
37. Feller, G.,, M. Thiry,, J.-L. Arpigny,, M. Mergeay, and, C. Gerday. 1990. Lipases from psychrotrophic Antarctic bacteria. FEMS Microbiol. Lett. 66:239244.
38. Feller, G.,, Z. Zekhnini,, J. Lamotte-Brasseur, and, C. Gerday. 1997. Enzyme from cold-adapted microorganisms. The class C β-lactamase from the Antarctic psychrophile Psychrobacter immobilis A5. Eur. J. Biochem. 244:186191.
39. Fernandes, S.,, B. Geueke,, O. Delgado,, J. Coleman, and, R. Hatti-Kaul. 2002. β-galactosidase from a cold-adapted bacterium: purification, characterization and application for lactose hydrolysis. Appl. Microbiol. Biotechnol. 58:313321.
40. Fitter, J.,, and J. Heberle. 2000. Structural equilibrium fluctuations in mesophilic and thermophilic α-amylase. Biophys. J. 79:16291636.
41. Galkin, A.,, L. Kulakova,, H. Ashida,, Y. Sawa, and, N. Esaki. 1999. Cold-adapted alanine dehydrogenase from two Antarctic bacterial strains: gene cloning, protein characterization, and comparison with mesophilic and thermophilic counterparts. Appl. Environ. Microbiol. 65:40144020.
42. Garcia-Viloca, M.,, J. Gao,, M. Karplus, and, D. G. Truhlar. 2004. How enzymes work: analysis by modern rate theory and computer simulations. Science 303:186195.
43. Garsoux, G.,, J. Lamotte-Brasseur,, C. Gerday, and, G. Feller. 2004. Kinetic and structural optimisation to catalysis at low temperatures in a psychrophilic cellulase from the Antarctic bacterium Pseudoalteromonas haloplanktis. Biochem. J. 384:247253.
44. Georlette, D.,, V. Blaise,, T. Collins,, S. D’Amico,, E. Gratia,, A. Hoyoux,, J.-C. Marx,, G. Sonan,, G. Feller, and, C. Gerday. 2004. Some like it cold: biocatalysis at low temperatures. FEMS Microbiol. Rev. 28:2542.
45. Georlette, D.,, B. Damien,, V. Blaise,, E. Depiereux,, V. N. Uversky,, C. Gerday, and, G. Feller. 2003. Structural and functional adaptations to extreme temperatures in psychrophilic, mesophilic and thermophilic DNA ligases. J. Biol. Chem. 278:3701537023.
46. Gerday, C.,, M. Aittaleb,, J.-L. Arpigny,, E. Baise,, J.-P. Chessa,, G. Garsoux,, I. Petrescu, and, G. Feller. 1997. Psychrophilic enzymes: a thermodynamic challenge. Biochim. Biophys. Acta. 1342:119131.
47. Gerday, C.,, M. Aittaleb,, M. Bentahir,, J.-P. Chessa,, P. Claverie,, T. Collins,, S. D’Amico,, J. Dumont,, G. Garsoux,, D. Georlette,, A. Hoyoux,, T. Lonhienne,, M.-A. Meuwis, and, G. Feller. 2000. Cold-adapted enzymes: from fundamentals to biotechnology. Trends Biotechnol. 18:103107.
48. Gerike, U.,, M. Danson,, N. J. Russell, and, D. Hough. 1997. Sequencing and expression of the gene encoding a cold-active citrate synthase from an Antarctic bacterium, strain DS2-3R. Eur. J. Biochem. 248:4957.
49. Gerike, U.,, M. J. Danson, and, D. W. Hough. 2001. Cold-active citrate synthase: mutagenesis of active-site residues. Protein. Engng. 14:655661.
50. Gianese, G.,, F. Bossa, and, S. Pascarella. 2002. Comparative structural analysis of psychrophilic and mesophilic and thermophilic enzymes. Proteins. 47:236249.
51. Giver, L.,, A. Gershenson,, P. Freskgard, and, F. Arnold. 1998. Directed evolution of a thermostable esterase. Proc. Natl. Acad. Sci. USA 95:1280912813.
52. Glansdorff, N.,, and Y. Xu. 2002. Microbial life at low temperatures/mechanisms of adaptation and extreme biotopes. Implications for exobiology and the origin of life. Rec. Res. Develop. Microbiol. 6:121.
53. Hata, K.,, R. Hono,, M. Fujisawa,, R. Kitahara,, Y. Kamatari,, K. Akasaka, and, X. Ying. 2004. High pressure NMR study of dihydrofolate reductase from a deep-sea bacterium Moritella profunda. Cell. Mol. Biol. 50:311316.
54. Hauksson, J. B.,, O. S. Andresson, and, B. Asgeirsson. 2000. Heat-labile bacterial alkaline phosphatase from a marine Vibrio sp. Enz. Microb. Technol. 27:6673.
55. Haynie, D. T. 2001. Collision theory, p. 261–262. In D. T. Haynie (ed.), Biological Thermodynamics, 1st ed. Cambridge University Press, Cambridge United Kingdom.
56. Helland, R.,, I. Leiros,, G. Berglund,, N. P. Willassen, and, A. O. Smalas. 1998. The crystal structure of anionic salmon trypsin in complex with bovine pancreatic trypsin inhibitor. Eur. J. Biochem. 256:317324.
57. Hernandez, G.,, F. E. Jenney,, M. W. Adams, and, D. M. Lemaster. 2000. Millisecond time scale conformational flexibility in a hyperthermophile at ambient temperature. Proc. Natl. Acad. Sci. USA 97:29622964.
58. Hiroki, T.,, B. Mikami, and, A. Yasuo. 2005. Crystal structure of cold-active protein–tyrosine phosphatase from a psychrophile, Shewanella sp. J. Biochem. (Tokyo) 137:6977.
59. Hollien, J.,, and S. Marqusee. 2002. Comparison of the folding processes of T. Thermophilus and E. coli ribonucleases H. J. Mol. Biol. 316:327340.
60. Hoyoux, A.,, V. Blaise,, T. Collins,, S. D’Amico,, E. Gratia,, A. L. Huston,, J.-C. Marx,, G. Sonan,, Y. Zeng,, G. Feller, and, C. Gerday. 2004. Extreme catalysts from low-temperature environments. J. Biosci. Bioeng. 98:317330.
61. Hoyoux, A.,, I. Jennes,, P. Dubois,, S. Genicot,, F. Dubail,, J.-M. Francois,, E. Baise,, G. Feller, and, C. Gerday. 2001. Cold-adapted β-galactosidase from the Antarctic psychrophile Pseudoalteromonas haloplanktis. Appl. Environ. Microbiol. 67:15291535.
62. Huston, A. L.,, B. B. Krieger-Brockett, and, J. Deming. 2000. Remarkably low temperature optima for extracellular enzyme activity from Artic bacteria and sea ice. Environ. Microbiol. 2:383388.
63. Ingraham, J. L.,, and J. L. Stokes. 1959. Psychrophilic bacteria. Bacteriol. Rev. 23:97108.
64. Jaenike, R. 1990. Protein structure and function at low temperatures. Philos. Trans. R. Soc. Lond. Series B.: Biol. Sci. 326:535551.
65. Jay, J. M. 1986. Characteristics and growth of psychrotrophic microorganisms. p. 579–592. In D. Van Nostrand (ed.), Modern Food Microbiology, 3rd ed. Reinhold Company, New-York.
66. Kimura, T.,, and K. Horikoshi. 1990. Characterization of pullulanhydrolysing enzyme from an alkali-psychrotrophic Micrococcus sp. Appl. Microbiol. Biotechnol. 34:5256.
67. Kramers, H. A. 1940. Brownian motion in a field of force and the diffusion model of chemical reactions. Physica. 7:284304.
68. Kumar, S.,, and R. Nussinov. 2004. Different roles of electrostatics in heat and in cold: adaptation by citrate synthase. Chem. Bio. Chem. 5:280290.
69. Kumar, S.,, T. Chung-Jung, and, R. Nussinov. 2002. Maximal stabilities of reversible two-state proteins. Biochemistry 41:53595374.
70. Leiros, I.,, E. Moe,, O. Lanes,, A. O. Smalas, and, N. P. Willassen. 2003. The structure of uracil-DNA glycosylase from Atlantic cod (Gadus morhua) reveals cold-adaptation features. Acta Crystallog. Sect.D. 59:13571365.
71. Liang, Z.,, I. Tsigos,, T. Lee,, V. Bouriotis,, K. Resing,, N. Ahn, and, J. Klinman. 2004. Evidence for increased local flexibility in psychrophilic alcohol dehydrogenase relative to its thermophilic homologue. Biochemistry 43:1467614683.
72. Lonhienne, T.,, C. Gerday, and, G. Feller. 2000. Psychrophilic enzymes: revisiting the thermodynamic parameters of activation may explain local flexibility. Biochim. Biophys. Acta. 1543:110.
73. Lonhienne, T.,, E. Baise,, G. Feller,, V. Bouriotis, and, C. Gerday. 2001a. Enzyme activity determination on macromolecular substrates by isothermal titration calorimetry: application to mesophilic and psychrophilic chitinases. Biochim. Biophys. Acta. 1545:349356.
74. Lonhienne, T.,, J. Zoidakis,, C. E. Vorgias,, G. Feller,, C. Gerday, and, V. Bouriotis. 2001b. Modular structure, local flexibility and cold-activity of a novel chitobiase from a psychrophilic Antarctic bacterium. J. Mol. Biol. 310:291297.
75. Makhtadze, G. I.,, and P. L. Privalov. 1994. Hydration effects in protein unfolding. Biophys. Chem. 51:291309.
76. Margesin, R.,, and F. Schinner. 1992. Extracellular protease production by psychrotrophic bacteria from glaciers. Intern. Biodet. Biodegr. 29:177189.
77. Marx, J.-C.,, V. Blaise,, T. Collins,, S. D’Amico,, D. Delille,, E. Gratia,, A. Hoyoux,, A. L. Huston,, G. Sonan,, G. Feller, and, C. Gerday. 2004. A perspective on cold enzymes: current knowledge and frequently asked questions. Cell. Mol. Biol. 50:643655.
78. Mastro, A. M.,, and A. D. Keith. 1984. Diffusion in the aqueous compartment. J. Cell Biol. 99:180187.
79. Mavromatis, K.,, I. Tsigos,, M. Tzanodaskalaki,, M. Kokkinidis, and, V. Bouriotis. 2002. Exploring the role of a glycine cluster in cold adaptation of an alkaline phosphatase. Eur. J. Biochem. 269:23302335.
80. Mavromatis, K.,, G. Feller,, M. Kokkinidis, and, V. Bouriotis. 2003. Cold adaptation of a psychrophilic chitinase: a mutagenesis study. Protein Engng. 16:497503.
81. Miyazaki, K.,, P. L. Wintrode,, R. A. Grayling,, D. N. Rubingh, and, F. Arnold. 2000. Directed evolution study of temperature adaptation in a psychrophilic enzyme. J. Mol. Biol. 297:10151026.
82. Mizuho, Y.,, S. Takehiko,, N. Katsutoshi, and, Y. Takada. 2004. Characterization of chimeric isocitrate dehydrogenase of a mesophilic nitrogen-fixing bacterium, Azobacter vinelandii, and a psychrophilic bacterium, Colwellia maris. Curr. Microbiol. 48:383388.
83. Mostafa, W. H.,, H. H. Radman, and, A. M. Hashem. 2003. Expression of cold adaptative enzymes of Pseudomonas fluorescens. New Egypt. J. Microbiol. 6:162187.
84. Narinx, E.,, E. Baise, and, C. Gerday. 1997. Subtilisin from psychrophilic Antarctic bacteria: characterization and site-directed mutagenesis of residues possibly involved in the adaptation to cold. Protein Engng. 10:12711279.
85. Okubo, Y.,, K. Yokoigawa,, N. Esaki,, K. Soda, and, H. Kawai. 1999. Characterization of psychrophilic alanine racemase from Bacillus psychrosaccharolyticus. Biochem. Biophys. Res. Comm. 256:333340.
86. Olufsen, M.,, A. O. Smalas,, E. Moe, and, B. O. Brandsdal. 2005. Increased flexibility as a strategy for cold adaptation. A comparative molecular dynamics study of cold- and warm-active uracil DNA glycosylase. J. Biol. Chem. 280:1804218048.
87. Pazgier, M.,, M. Turkiewicz,, H. Kalinowska, and, S. Bielicki. 2003. The unique cold-adapted extracellular subtilase from psychrophilic yeast Leucosporidium antarcticum. J. Molecul. Cat. B. 21:3942.
88. Pelzer, H.,, and E. Wigner. 1932. Velocity coefficient of interchanges reactions. Z. Phys. Chem. B15:445471.
89. Petrescu, I.,, J. Lamotte-Brasseur,, J.-P. Chessa,, P. Ntarima,, M. Claeyssens,, B. Devreese,, G. Marino, and, C. Gerday. 2000. Xylanase from psychrophilic yeast Cryptococcus adeliae. Extremophiles 4:137144.
90. Ratkowsky, D. A.,, J. Olley, and, T. Ross. 2005. Unifying temperature effects on the growth rate of bacteria and the stability of globular proteins. J. Theor. Biol. 233:351362.
91. Roovers, M.,, R. Sanchez,, C. Legrain, and, N. Glansdorff. 2001. Experimental evolution of enzyme temperature activity profile selection in vivo and characterization of low-temperature adapted mutants of Pyrococcus furiosus ornithine carbamoyl transferase. J. Bacteriol. 183:11011105.
92. Russell, N. J. 1990. Cold-adaptation of microorganisms. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 326:595611.
93. Russell, N. J. 2000. Toward a molecular understanding of cold activity of enzymes from psychrophiles. Extremophiles 4:8390.
94. Russell, R. J.,, U. Gerike,, M. J. Danson,, D. W. Hough, and, G. L. Taylor. 1998. Structural adaptations of the cold-active citrate synthase from an Antarctic bacterium. Structure 6:351361.
95. Shoichet, B. K.,, W. A. Baase,, R. Kuroki, and, B. W. Matthews. 1995. A relationship between protein stability and protein function. Proc. Natl. Acad. Sci. USA 92:452456.
96. Smalas, A. O.,, H. K. Leiros,, V. Os, and, N. P. Willassen. 2000. Cold-adapted enzymes. Biotechnol. Ann. Rev. 6:157.
97. Siddiqui, K. S.,, S. A. Bokhari,, A. J. Afzal, and, S. Singh. 2004. A novel thermodynamic relationship based on Kramers theory for studying enzyme kinetics under high viscosity. IUBMB Life 56:403407.
98. Skalova, T.,, J. Dohnalek,, V. Spiwok,, P. Lipovova,, E. Vondrackova,, H. Petrokova,, J. Duskova,, H. Strnad,, B. Kralova, and, J. Hasek. 2005. Cold-active β-galactosidase from Arthrobacter sp. C2-2 forms compact 660kDa hexamers: crystal structure at 1.9 Å resolution. J. Mol. Biol. 353:282294.
99. Sun-Yong, K.,, H. Kwang-Yeon,, K. Sung-Hou,, S. Ha-Chin,, H. Ye-Sun, and, C. Yunge. 1999. Structural basis for cold adaptation. Sequence, biochemical properties, and crystal structure of malate dehydrogenase from a psychrophile Aquaspirillium arcticum. J. Biol. Chem. 274:1176111767.
100. Suzuki, T.,, T. Nakayama,, T. Kurihara,, T. Nishino, and, N. Esaki. 2002a. Primary structure and catalytic properties of a cold-active esterase from a psychrotroph, Acinetobacter sp. Strain no.6. isolated from Siberian soil. Biosci. Biotechnol. Biochem. 66:16821690.
101. Suzuki, T.,, M. Yasugi,, F. Arisaka,, T. Oshima, and, A. Yamagishi. 2002b. Cold-adaptation mechanism of mutant enzymes of 3-isopropylmalate dehydrogenase from Thermus thermophilus. Protein Engng. 15:471476.
102. Svingor, A.,, J. Kardos,, I. Hadju,, A. Nemeth, and, P. Zavodszky. 2001. A better enzyme to cope with cold. Comparative flexibility studies on psychrotrophic, mesophilic, and thermophilic IPMDHS. J. Biol. Chem. 276:2812128125.
103. Taguchi, S.,, S. Komada, and, H. Momose. 2000. The complete amino acid substitutions at position 131 that are positively involved in cold adaptation of subtilisin BPN′. Appl. Environ. Microbiol. 66:14101415.
104. Tehei, M.,, B. Franzetti,, D. Madern,, M. Ginzburg,, B. Z. Ginzburg,, M.-T., Giudici-Orticoni,, M. Bruschi, and, G. Zaccai. 2004. Adaptation to extreme environments: macromolecular dynamics in bacteria compared in vivo by neutron scattering. EMBO Rep. 5:6670.
105. Thomas, T.,, and R. Cavicchioli. 2000. Effect of temperature on stability and activity of elongation factor 2 proteins from Antarctic and thermophilic methanogens. J. Bacteriol. 182:13281332.
106. Tindbaek, N.,, A. Svendsen,, P. Oestergaard, and, H. Draborg. 2004 Engineering a substrate-specific cold-adapted subtilisin. Protein Engng. 17:149156.
107. Tsigos, I.,, K. Mavromatis,, M. Tzanodaslaki,, C. Pozidis,, M. Kokkinidis, and, V. Bouriotis. 2001. Engineering the properties of a cold-active enzyme through rational redesign of the active site. Eur. J. Biochem. 268:50745080.
108. Van Petegem, F.,, T. Collins,, M.-A. Meuwis,, C. Gerday,, G. Feller, and, J. Van Beeumen. 2003. The structure of a cold-adapted family 8 xylanase at 1.3 A resolution. Structural adaptations to cold and investigation of the active site. J. Biol. Chem. 278:75317539.
109. Van Truong, L.,, H. Tuyen,, E. Helmke,, L. Tran Binh, and, T. Schweder. 2001. Cloning of two pectate lyase genes from the marine Antarctic bacterium Pseudoalteromonas haloplanktis strain ANT/505 and characterization of the enzymes. Extremophiles 5:3544.
110. Vieille, C.,, and G. J. Zeikus. 2001. Hyperthermophilic enzymes: sources, uses and molecular mechanisms for thermostability. Microbiol. Mol. Rev. 65:143.
111. Vihinen, M. 1987. Relationship of protein flexibility to thermostability. Protein Engng. 1:477480.
112. Violot, S.,, N. Aghajari,, M. Czjzek,, G. Feller,, G. K. Sonan,, P. Gouet,, C. Gerday,, R. Haser, and, V. Receveur-Bréchot. 2005. Structure of a full length psychrophilic cellulase from Pseudoalteromonas haloplanktis revealed by X-ray diffraction and small angle X-ray scattering. J. Mol. Biol. 348:12111224.
113. Watanabe, S.,, Y. Takada, and, N. Fukunaga. 2001. Purification and characterization of a cold-adapted isocitratelyase and a malate synthase from Colwellia maris, a psychrophilic bacterium. Biosci. Biotechnol. Biochem. 65:10951103.
114. Watanabe, S.,, and Y. Takada. 2004. Amino acid residues involved in cold-adaptation of isocitrate lyase from a psychrophilic bacterium, Colwellia maris. Microbiology (Reading, UK). 150:33933403.
115. Watanabe, S.,, Y. Yasutake,, Y. I. Tanaka, and, Y. Takada. 2005. Elucidation of stability determinant of cold-adapted monomeric isocitratedehydrogenase from a psychrophilic bacterium Colwellis maris, by construction of chimeric enzymes. Microbiology 151:10831094.
116. Xu, Y.,, G. Feller,, C. Gerday, and, N. Glansdorff. 2003a. Metabolic enzymes from psychrophilic bacteria: challenge of adaptation to low temperatures in ornithine carbamoyltransferase from Moritella abyssi. J. Bacteriol. 185:21612168.
117. Xu, Y.,, G. Feller,, C. Gerday, and, N. Glansdorff. 2003b. Moritella cold-active dihydrofolate reductase: are there natural limits to optimisation of catalytic efficiency at low temperature? J. Bacteriol. 185:55195526.
118. Xu, Y.,, Y. Nogi,, C. Kato,, Z. Liang,, H. J. Ruger,, D. De Kegel, and, N. Glansdorff. 2003c. Moritella profunda sp. Nov.and Moritella abysi sp. Nov., two psychropiezophilic organisms isolated from deep Atlantic sediments. Int. J. Syst. Evol. Microbiol. 53:533538.
119. Yamamoto, T.,, and G. Kunihiko. 2003. Study of flexibility of protein by mass spectrometry. J. Mass Spectro. Soc. Jap. 51:412414.
120. Yumoto, I.,, D. Ichihashi,, H. Iwata,, A. Istokovics,, N. Ichise,, H., Matsuyama,, H. Okuyama, and, K. Kawasaki. 2000. Purification and characterization of a catalase from the facultatively psychrophilic bacterium Vibrio rumiensis S-1 exhibiting high catalase activity. J. Bacteriol. 182:19031909.
121. Zavodszky, P.,, J. Kardos,, A. Svingor, and, G. A. Petsko. 1998. Adjustment of conformational flexibility is a key event in the thermal adaptation of proteins. Proc. Natl. Acad. Sci. USA 95:74067411.
122. Zecchinon, L.,, P. Claverie,, T. Collins,, S. D’Amico,, D. Delille,, G. Feller,, D. Georlette,, E. Gratia,, A. Hoyoux,, M.-A. Meuwis,, G. Sonan, and, C. Gerday. 2001. Did psychrophilic enzymes really win the challenge? Extremophiles 5:313321.


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Table 1.

Catalytic properties and activation parameters of various psychrophile enzymes compared to those of their mesophilic counterparts

Citation: Collins T, D’Amico S, Marx J, Feller G, Gerday C. 2007. Cold-Adapted Enzymes, p 165-179. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch13

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