Psychrophilic enzymes: Hot topics in cold adaptation

[en] More than three-quarters of the Earth's surface is occupied by cold ecosystems, including the ocean depths, and polar and alpine regions. These permanently cold environments have been successfully colonized by a class of extremophilic microorganisms that are known as psychrophiles (which literally means cold-loving). The ability to thrive at temperatures that are close to, or below, the freezing point of water requires a vast array of adaptations to maintain the metabolic rates and sustained growth compatible with life in these severe environmental conditions.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

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 :

Psychrophilic enzymes: Hot topics in cold adaptation

Publication date :

December 2003

Journal title :

Nature Reviews. Microbiology

ISSN :

1740-1526

eISSN :

1740-1534

Publisher :

Nature Publishing Group, London, United Kingdom

Volume :

Issue :

Pages :

200-208

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 26 January 2010

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913

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Bibliography

Yayanos, A. A. Microbiology to 10, 500 meters in the deep sea. Annu. Rev. Microbiol. 49, 777-805 (1995).
Staley, J. T. & Gosink, J. J. Poles apart: biodiversity and biogeography of sea ice bacteria. Annu. Rev. Microbiol. 53, 189-215 (1999).
Carpenter, E. J., Lin, S. & Capone, D. G. Bacterial activity in South Pole snow. Appl. Environ. Microbiol. 66, 4514-4517 (2000).
Friedmann, E. I. Endolithic microorganisms in the Antarctic cold desert. Science 215, 1045-1053 (1982).
Morita, R. Y. Psychrophilic bacteria. Bacteriol. Rev. 39, 144-167 (1975).
Russell, N. J. Cold adaptation of microorganisms. Phil. Trans. R. Soc. Lond. B. 326, 595-611 (1990).
Gounot, A. M. Bacterial life at low temperature: physiological aspects and biotechnological implications. J. Appl. Bacterid 71, 386-397 (1991).
Cold-adapted Organisms: Ecology, Physiology, Enzymology and Molecular Biology (eds Margesin, R. & Schinner, F.) (Springer, Heidelberg, 1999).
Allen, D., Huston, A. L., Weels, L. E. & Deming, J. W. in Encyclopedia of Environmental Microbiology Vol. 1 (ed. Bitton, G.) 1-17 (John Wiley and Sons, New York, (2001).
Deming, J. W. Psychrophiles and polar regions. Curr. Opin. Microbiol. 5, 301-309 (2002).
Margesin, R., Feller, G., Gerday, C. & Russell, N. J. in Encyclopedia of Environmental Microbiology.Vol. 2 (ed. Bitton, G.), 871-885 (John Wiley and Sons, New York, 2002).
Saunders, N. F. et al. Mechanisms of thermal adaptation revealed from the genomes of the Antarctic Archaea Methanogenium frigidum and Methanococcoides burtonii. Genome Res. 13, 1580-1588 (2003).
Somero, G. N. Proteins and temperature. Annu. Rev. Physiol. 57, 43-68 (1995).
Low, P. S., Bada, J. L. & Somero, G. N. Temperature adaptation of enzymes: roles of the free energy, the enthalpy, and the entropy of activation. Proc. Natl Acad. Sci. USA 70, 430-432 (1973).
Lonhienne, T., Gerday, C. & Feller, G. Psychrophilic enzymes: revisiting the thermodynamic parameters of activation may explain local flexibility. Biochim. Biophys. Acta 1543, 1-10 (2000).
D'Amico, S., Marx, J. C., Gerday, C. & Feller, G. Activity-stability relationships in extremophilic enzymes. J. Biol. Chem. 278, 7891-7896 (2003).
Collins, T, Meuwis, M. A., Gerday, C. & Feller, G. Activity, stability and flexibility in glycosidases adapted to extreme thermal environments. J. Mol. Biol. 328, 419-428 (2003).
Fields, P A. & Somero, G. N. Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A4orthologs of Antarctic notothenioid fishes. Proc. Natl A cad. Sci. USA 95, 11476-11481 (1998).
Xu, Y., Feller, G., Gerday, C. & 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).
Lonhienne, T. et al. Modular structure, local flexibility and cold-activity of a novel chitobiase from a psychrophilic Antarctic bacterium. J. Mol. Biol. 310, 291-297 (2001).
Aghajari, N., Feller, G., Gerday, C. & Haser, R. Structures of the psychrophilic Alteromonas haloplanctis a-amylase give insights into cold adaptation at a molecular level. Structure 6, 1503-1516 (1998).
Holland, L. Z., McFall-Ngai, M. & Somero, G. N. Evolution of lactate dehydrogenase-A homologs of barracuda fishes (genus Sphyraena) from different thermal environments: differences in kinetic properties and thermal stability are due to amino acid substitutions outside the active site. Biochemistry 36, 3207-3215 (1997).
Russell, R. J., Gerike, U., Danson, M. J., Hough, D. W. & Taylor, G. L. Structural adaptations of the cold-active citrate synthase from an Antarctic bacterium. Structure 6, 351-361 (1998).
Aghajari, N. et al. Crystal structures of a psychrophilic metalloprotease reveal new insights into catalysis by cold- adapted proteases. Proteins 50, 636-647 (2003).
Kim, S. Y. et al. 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).
Smalas, A. O., Leiros, H. K., Os, V. & Willassen, N. P Cold- adapted enzymes. Biotechnol. Annu. Rev. 6, 1-57 (2000).
Brandsdal, B. O., Smalas, A. O. & Aqvist, J. Electrostatic effects play a central role in cold adaptation of trypsin. FEBS Lett. 499, 171-175 (2001).
Zavodszky, P., Kardos, J., Svingor, L. A. & 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).
Svingor, A., Kardos, J., Hajdu, I., Nemeth, A. & 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).
Fields, P. A. Protein function at thermal extremes: balancing stability and flexibility. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 129, 417-431 (2001).
Smalas, A. O., Heimstad, E. S., Hordvik, A., Willassen, N. P & Male, R. Cold adaption of enzymes: structural comparison between salmon and bovine trypsins. Proteins 20, 149-166 (1994).
Russell, N. J. Toward a molecular understanding of cold activity of enzymes from psychrophiles. Extremophiles 4, 83-90 (2000).
Bell, G. S. et al. Stepwise adaptations of citrate synthase to survival at life's extremes. From psychrophile to hyperthermophile. Eur. J. Biochem. 269, 6250-6260 (2002).
Leiros, H. K., Willassen, N. P. & Smalas, A. O. Residue determinants and sequence analysis of cold-adapted trypsins. Extremophiles 3, 205-219 (1999).
Schroder-Leiros, H. K., Willassen, N. P. & Smalas, A. O. Structural comparison of psychrophilic and mesophilic trypsins. Elucidating the molecular basis of cold-adaptation. Eur. J. Biochem. 267, 1039-1049 (2000).
Gianese, G., Argos, P & Pascarella, S. Structural adaptation of enzymes to low temperatures. Protein Enq. 14, 141-148 (2001).
Gianese, G., Bossa, F. & Pascarella, S. Comparative structural analysis of psychrophilic and meso- and thermophilic enzymes. Proteins 47, 236-249 (2002).
Feller, G., d'Amico, D. & Gerday, C. Thermodynamic stability of a cold-active a-amylase from the Antarctic bacterium Alteromonas haloplanctis. Biochemistry.38, 4613-4619 (1999)
D'Amico, S., Gerday, C. & Feller, G. Structural determinants of cold adaptation and stability in a large protein. J. Biol. Chem. 276, 25791-25796 (2001).
Feller, G., Le Bussy, O. & Gerday, C. Expression of psychrophilic genes in mesophilic hosts: assessment of the folding state of a recombinant a-amylase. Appl. Environ. Microbiol. 64, 1163-1165 (1998).
Makhatadze, G. I. & Privalov, P L. Energetics of protein structure. Adv. Protein Chem. 47, 307-425 (1995).
Zecchinon, L. et al. Did psychrophilic enzymes really win the challenge? Extremophiles 5, 313-321 (2001).
D'Amico, S., Gerday, C. & Feller, G. Dual effects of an extra disulfide bond on the activity and stability of a cold-adapted a-amylase. J. Biol. Chem. 277, 46110-46115 (2002).
Narinx, E., Baise, E. & Gerday, C. Subtilisin from psychrophilic antarctic bacteria: characterization and site- directed mutagenesis of residues possibly involved in the adaptation to cold. Protein Eng. 10, 1271-1279 (1997).
Gerike, U., Danson, M. J. & Hough, D. W. Cold-active citrate synthase: mutagenesis of active-site residues. Protein Eng. 14, 655-661 (2001).
Tsigos, I. et al. Engineering the properties of a cold active enzyme through rational redesign of the active site. Eur. J. Biochem. 268, 5074-5080 (2001).
Ohtani, N., Haruki, M., Morikawa, M. & Kanaya, S. Heat labile ribonuclease HI from a psychrotrophic bacterium: gene cloning, characterization and site-directed mutagenesis. Protein Eng. 14, 975-982 (2001).
Mavromatis, K., Tsigos, I., Tzanodaskalaki, M., Kokkinidis, M. & Bouriotis, V. Exploring the role of a glycine cluster in cold adaptation of an alkaline phosphatase. Eur. J. Biochem. 269, 2330-2335 (2002).
Wintrode, P L. & Arnold, F. H. Temperature adaptation of enzymes: lessons from laboratory evolution. Adv. Protein Chem. 55, 161-225 (2000).
Wintrode, P L., Miyazaki, K. & Arnold, F. H. Cold adaptation of a mesophilic subtilisin-like protease by laboratory evolution. J. Biol. Chem. 275, 31635-31640 (2000).
Miyazaki, K., Wintrode, P. L., Grayling, R. A., Rubingh, D. N. & Arnold, F. H. Directed evolution study of temperature adaptation in a psychrophilic enzyme. J. Mol. Biol. 297, 1015-1026 (2000).
Bentahir, M. et al. Structural, kinetic, and calorimetric characterization of the cold-active phosphoglycerate kinase from the antarctic Pseudomonassp. TACII18. J. Biol. Chem. 275, 11147-11153 (2000).
Claverie, P, Vigano, C., Ruysschaert, J. M., Gerday, C. & Feller, G. The precursor of a psychrophilic a-amylase: structural characterization and insights into cold adaptation. Biochim. Biophys. Acta 1649, 119-122 (2003).
D'Amico, S. et al. Molecular basis of cold adaptation. Phil. Trans. R. Soc. Lond. B. 357, 917-925 (2002).
Roovers, M., Sanchez, R., Legrain, C. & Glansdorff, N. Experimental evolution of enzyme temperature activity profile: selection in vivo and characterization of low- temperature-adapted mutants of Pyrococcus furiosus ornithine carbamoyltransferase. J. Bacteriol. 183, 1101-1105 (2001).
Giver, L., Gershenson, A., Freskgard, P. O. & Arnold, F. H. Directed evolution of a thermostable esterase. Proc. Natl Acad. Sci. USA 95, 12809-12813 (1998).
Cherry, J. R. et al. Directed evolution of a fungal peroxidase. Nature Biotechnol. 17, 379-384 (1999).
Georlette, D. et al. Structural and functional adaptations to extreme temperatures in psychrophilic, mesophilic and thermophilic DNA ligases. J. Biol. Chem. 278, 37015-37023 (2003).
Jaenicke, R. Do ultrastable proteins from hyperthermophiles have high or low conformational rigidity? Proc. Natl Acad. Sci. USA 97, 2962-2964 (2000).
Hernandez, G., Jenney, F. E. Jr, Adams, M. W. & LeMaster, D. M. Millisecond time scale conformational flexibility in a hyperthermophile protein at ambient temperature. Proc. Natl Acad. Sci. USA 97, 3166-3170 (2000).
Tehei, M., Madern, D., Pfister, C. & 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).
Gabel, F. et al. Protein dynamics studied by neutron scattering. Q. Rev. Biophys. 35, 327-367 (2002).
Davail, S., Feller, G., Narinx, E. & Gerday, C. Cold adaptation of proteins. Purification, characterization, and sequence of the heat-labile subtilisin from the Antarctic psychrophile Bacillus TA41. J. Biol. Chem. 269, 17448-17453 (1994).
Lonhienne, T et al. Cloning, sequences, and characterization of two chitinase genes from the Antarctic Arthrobacter sp. strain TAD20: isolation and partial characterization of the enzymes. J. Bacteriol. 183, 1773-1779 (2001).
Thomas, T. & Cavicchioli, R. Archaeal cold-adapted proteins: structural and evolutionary analysis of the elongation factor 2 proteins from psychrophilic, mesophilic and thermophilic methanogens. FEBS Lett. 439, 281-286 (1998).
Thomas, T. & Cavicchioli, R. Effect of temperature on stability and activity of elongation factor 2 proteins from Antarctic and thermophilic methanogens. J. Bacteriol. 182, 1328-1332 (2000).
Thomas, T., Kumar, N. & Cavicchioli, R. Effects of ribosomes and intracellular solutes on activities and stabilities of elongation factor 2 proteins from psychrotolerant and thermophilic methanogens. J. Bacteriol. 183, 1974-1982 (2001).
Siddiqui, K. S., Cavicchioli, R. & Thomas, T. Thermodynamic activation properties of elongation factor 2 (EF-2) proteins from psychrotolerant and thermophilic Archaea. Extremophiles 6, 143-150 (2002).
Deegenaars, M. L. & Watson, K. Heat shock response in psychrophilic and psychrotrophic yeast from Antarctica. Extremophiles 2, 41-49 (1998).
Petrescu, I. et al. Xylanase from the psychrophilic yeast Cryptococcus adeliae. Extremophiles 4, 137-144 (2000).
Sabri, A. et al Influence of moderate temperatures on myristoyl-CoA metabolism and acyl-CoA thioesterase activity in the psychrophilic antarctic yeast Rhodotorula aurantiaca. J. Biol Chem. 276, 12691-12696 (2001).
Loppes, R., Devos, N., Willem, S., Bartelemy, P. & Matagne, R. F. Effect of temperature on two enzymes from a psychrophilic Chloromonas (chlorophyta). J. Phycol. 32, 276-278 (1996).
Devos, N., Ingouff, M., Loppes, R. & Matagne, R. F. Rubisco adaptation to low temperatures: a comparative study in psychrophilic and mesophilic unicellular algae. J. Phycol. 34, 655-660 (1998).
Willem, S. et al. Protein adaptation to low temperatures: a comparative study of a-tubulin sequences in mesophilic and psychrophilic algae. Extremophiles 3, 221-226 (1999).
de Backer, M. et al. The 1.9 A crystal structure of heat-labile shrimp alkaline phosphatase. J. Mol. Biol. 318, 1265-1274 (2002).
Eastman, J. T. Antarctic Fish Biology: Evolution in a Unique Environment (Academic Press, San Diego, 1993).
Fishes of Antarctica: a Biological Overview (eds di Prisco, G., Pisano, E. & Clarke, A.) (Springer, Milan, 1998).
Orange, N. Growth temperature regulates the induction of β-lactamase in Pseudomonas fluorescens through modulation of the outer membrane permeation of a β -lactam-inducing antibiotic. Microbiology 140, 3125-3130 (1994).
Feller, G. et al. Temperature dependence of growth, enzyme secretion and activity of psychrophilic Antarctic bacteria. Appl. Microbiol. Biotechnol. 41, 477-479 (1994).
De, E. et al. Growth temperature dependence of channel size of the major outer-membrane protein (OprF) in psychrotrophic Pseudomonas fluorescens strains. Microbiology 143, 1029-1035 (1997).
Cavicchioli, R. Extremophiles and the search for extraterrestrial life. Astrobiology. 2, 281-292 (2002).
Glansdorff, N. & Xu, Y. Microbial life at low temperatures: mechanisms of adaptation and extreme biotopes. Implications for exobiology and the origin of life. Recent Res. Dev. Microbiol. 6, 1-21 (2002).
Russell, N. J. & Hamamoto, T. in Extremophiles: Microbial Life in Extreme Environments (eds Horikoshi, K. & Grant, D.) 25-45 (Wiley, New York, 1998).
Russell, N. J. Psychrophilic bacteria: molecular adaptations of membrane lipids. Comp. Biochem. Physiol. Physiol. 118, 489-493 (1997).
Jagannadham, M. V. et al. Carotenoids of an Antarctic psychrotolerant bacterium, Sphingobacterium antarcticus, and a mesophilic bacterium, Sphingobacterium multivorum. Arch. Microbiol. 173, 418-424 (2000).
Fong, N. J., Burgess, M. L., Barrow, K. D. & Glenn, D. R. Carotenoid accumulation in the psychrotrophic bacterium Arthrobacter agilisin response to thermal and salt stress. Appl. Microbiol. Biotechnol. 56, 750-756 (2001).
Michel, V. et al. The cold shock response of the psychrotrophic bacterium Pseudomonas fragiinvolves four low-molecular-mass nucleic acid-binding proteins. J. Bacterid. 179, 7331-7342 (1997).
Tendeng, C. et al. A novel H-NS-like protein from an Antarctic psychrophilic bacterium reveals a crucial role for the N-terminal domain in thermal stability. J. Biol. Chem. 278, 18754-18760 (2003).
Cavicchioli, R., Thomas, T. & Curmi, P M. G. Cold stress response in archaea. Extremophiles4, 321-331 (2000).
Lim, J., Thomas, T. & Cavicchioli, R. Low temperature regulated DEAD-box RNA helicase from the Antarctic archaeon, Methanococcoides burtonii. J. Mol. Biol. 297, 553-567 (2000).
Dalluge, J. J. et al. Posttranscriptional modification of tRNA in psychrophilic bacteria. J. Bacteriol. 179, 1918-1923 (1997).
Hebraud, M. & Potier, P. in Cold Shock, Response and Adaptation (eds Inouye, M. & Yamanaka, K.) 41-60 (Horizon Scientific, UK, 2000).
Hebraud, M., Dubois, E., Potier, P. & Labadie, J. Effect of growth temperatures on the protein levels in a psychrotrophic bacterium, Pseudomonas fragi. J. Bacteriol. 176, 4017-4024 (1994).
Berger, F., Morellet, N., Menu, F. & Potier, P. Cold shock and cold acclimation proteins in the psychrotrophic bacterium Arthrobacter globiformis SI55. J. Bacteriol. 178, 2999-3007 (1996).
Berger, F., Normand, P. & Potier, P. capA, a cspA-like gene that encodes a cold acclimation protein in the psychrotrophic bacterium Arthrobacter globiformis SI55. J. Bacteriol. 179, 5670-5676 (1997).
Jia, Z., DeLuca, C. I., Chao, H. & Davies, P. L. Structural basis for the binding of a globular antifreeze protein to ice. Nature 384, 285-288 (1996).
Russell, N. J. Molecular adaptations in psychrophilic bacteria: potential for biotechnological applications. Adv. Biochem. Eng. Biotechnol. 61, 1-21 (1998).
Margesin, R. & Schinner, F. Biotechnological Applications of Cold-Adapted Organisms (Springer, Heidelberg, 1999).
Gerday, C. et al. Cold-adapted enzymes: from fundamentals to biotechnology. Trends Biotechnol. 18, 103-107 (2000).
Cavicchioli, R., Siddiqui, K. S., Andrews, D. & Sowers, K. R. Low-temperature extremophiles and their applications. Curr. Opin. Biotechnol. 13, 253-261 (2002).
Kobori, H., Sullivan, C. W. & Shizuya, H. Heat-labile alkaline phosphatase from Antarctic bacteria: rapid 5' end labelling of nucleic acids. Proc. Natl Acad. Sci. USA 81, 6691-6695 (1984).
Tutino, M. L. et al. A novel replication element from an Antarctic plasmid as a tool for the expression of proteins at low temperature. Extremophiles 5, 257-264 (2001).
Feller, G. et al. Purification, characterization and nucleotide sequence of the thermolabile a-amylase from the Antarctic psychrotroph Alteromonas haloplanctis A23. J. Biol. Chem. 267, 5217-5221 (1992).