Polar and other low temperature environments are characterized by a low content in energy and this factor has a strong incidence on living organisms which populate these rather common habitats. Indeed, low temperatures have a negative effect on ectothermic populations since they can affect their growth, reaction rates of biochemical reactions, membrane permeability, diffusion rates, action potentials, protein folding, nucleic acids dynamics and other temperature-dependent biochemical processes. Since the discovery that these ecosystems, contrary to what was initially expected, sustain a rather high density and broad diversity of living organisms, increasing efforts have been dedicated to the understanding of the molecular mechanisms involved in their successful adaptation to apparently unfavorable physical conditions. The first question that comes to mind is: How do these organisms compensate for the exponential decrease of reaction rate when temperature is lowered? As most of the chemical reactions that occur in living organisms are catalyzed by enzymes, the kinetic and thermodynamic properties of cold-adapted enzymes have been investigated. Presently, many crystallographic structures of these enzymes have been elucidated and allowed for a rather clear view of their adaptation to cold. They are characterized by a high specific activity at low and moderate temperatures and a rather low thermal stability, which induces a high flexibility that prevents the freezing effect of low temperatures on structure dynamics. These enzymes also display a low activation enthalpy that renders them less dependent on temperature fluctuations. This is accompanied by a larger negative value of the activation entropy, thus giving evidence of a more disordered ground state. Appropriate folding kinetics is apparently secured through a large expression of trigger factors and peptidyl–prolyl cis/ trans-isomerases.
References
[1]
Brinkmeyer, R.; Knittel, K.; Jürgens, J.; Weyland, H.; Amann, R.; Helmke, E. Diversity and structure of bacterial communities in Arctic versus Antarctic pack ice. Appl. Envirom. Microbiol. 2003, 69, 6610–6619, doi:10.1128/AEM.69.11.6610-6619.2003.
Steven, B.; Briggs, S.; McKay, C.P.; Pollard, W.H.; Greer, C.W.; Whyte, L.G. Characterization of the microbial diversity in a permafrost sample from the Canadian high Arctic using culture-dependent and culture-independent methods. FEMS Microbiol. Ecol. 2007, 59, 513–523, doi:10.1111/j.1574-6941.2006.00247.x.
[4]
Shivagi, S.; Kumari, K.; Kishore, K.H.; Pindi, P.K.; Rao, P.S.; Srivinas, T.N.R.; Asthana, R.; Ravindra, R. Vertical distribution of bacteria in a lake sediment from Antarctica by culture-independent and culture-dependent approaches. Res. Microbiol. 2011, 162, 191–203, doi:10.1016/j.resmic.2010.09.020.
[5]
Lo Giudice, A.; Caruso, C.; Mangano, S.; Bruni, V.; De Domenico, M.; Michaud, L. Marine bacterioplankton diversity and community composition in an Antarctic coastal environment. Microbiol. Ecol. 2012, 63, 210–223, doi:10.1007/s00248-011-9904-x.
[6]
Kirby, B.M.; Easton, S.; Tuffin, I.M.; Cowan, D.A. Bacterial diversity in polar habitats. In PolarMicrobiology. Life in a Deep Freeze; Miller, R.V., Whyte, L.G., Eds.; ASM Press: Washington DC, USA, 2012; Volume Chapter 1, p. 3.
[7]
Collins, T.; D’Amico, S.; Marx, J.C.; Feller, G.; Gerday, C. Cold-adapted enzymes. In Physiology and Biochemistry of Extremophiles; Gerday, C.H., Glansdorff, N., Eds.; ASM Press: Washington DC, USA, 2007; Volume Chapter 13, p. 165.
[8]
Garcia-Viloca, M.; Gao, J.; Karplus, M.; Truhlar, D.G. How enzymes work: Analysis by modern rate theory and computer simulation. Science 2004, 303, 186–195, doi:10.1126/science.1088172.
[9]
Demchenko, A.P.; Rusyn, O.I.; Saburova, E.A. Kinetics of the lactate dehydrogenase reaction in high viscosity media. Biochim. Biophys. Acta 1989, 998, 196–203, doi:10.1016/0167-4838(89)90273-2.
[10]
Mastro, A.M.; Keith, A.D. Diffusion in the aqueous compartment. J. Cell Biol. 1984, 99, 180–187, doi:10.1083/jcb.99.1.180s.
[11]
Siddiqui, K.S.; Bokhari, S.A.; Afzal, A.J.; Singh, S. A novel thermodynamic relationship based on Kramers theory for studying enzyme kinetics under high viscosity. IUBMB Life 2004, 56, 403–407, doi:10.1080/15216540400003052.
[12]
Feller, G.; Lonhienne, T.; Deroanne, C.; Libioulle, C.; Van Beeumen, J.; Gerday, C. Purification, characterization, and nucleotide sequence of the thermolabile α-amylase from the Antarctic psychrotroph Alteromonas. haloplanktis A23. J. Biol. Chem. 1992, 267, 5217–5221.
[13]
Kobori, H.; Sullivan, C.W.; Shizuya, H. Heat-labile alkaline phosphatase from Antarctic bacteria: Rapid 5' end-labeling of nucleic acid. Proc. Natl. Acad. Sci. USA 1984, 81, 6691–6695, doi:10.1073/pnas.81.21.6691.
[14]
De Santi, C.; Tutino, M.L.; Mandrich, L.; Giuliani, M.; Parrilli, E.; Del Vecchio, P.; De Pascale, D. The hormone-sensitive lipase from Psychrobacter. sp. TA144: New insight in the structural/functional characterization. Biochimie 2010, 92, 949–957, doi:10.1016/j.biochi.2010.04.001.
[15]
Simpson, P.J.L.; Codd, R. Cold adaptation of the mononuclear molybdoenzyme periplasmic nitrate reductase from the Antarctic bacterium Shewanella. gelidimarina.. Biochem. Biophys. Res. Comm. 2011, 414, 783–788, doi:10.1016/j.bbrc.2011.10.003.
[16]
Angelaccio, S.; Florio, R.; Consalvi, V.; Festa, G.; Pascarella, P. Serine hydroxymethyltransferase from the cold adapted microorganism Psychromonas. ingrahamii: A low temperature active enzyme with broad specificity. Int. Mol. Sci. 2012, 13, 1314–1326, doi:10.3390/ijms13021314.
[17]
D’Amico, S.; Gerday, C.; Feller, G. Structural determinants of cold adaptation and stability in a large protein. J. Biol. Chem. 2001, 276, 25791–25796, doi:10.1074/jbc.M102741200.
[18]
Birolo, M.; Tutino, L. Aspartate aminotransferase from the Antarctic bacterium Pseudoalteromonas. haloplanktis TAC 125. Cloning, expression, properties, and molecular modelling. Eur. J. Biochem. 2000, 267, 2790–2802, doi:10.1046/j.1432-1327.2000.01299.x.
[19]
Sun, K.; Camardella, L.; Di Prisco, G.; Hervé, G. Properties of aspartate transcarbamylase from TAD1, a psychrophilic bacterial strain isolated from Antarctica. FEMS Microbiol. Lett. 1998, 164, 375–382, doi:10.1111/j.1574-6968.1998.tb13112.x.
[20]
Gerike, U.; Danson, M.J.; Russell, N.J.; Hough, D.W. Sequencing and expression of the gene encoding a cold-active citrate synthase from an Antarctic bacterium strain DS-3R. Eur. J. Biochem. 1997, 248, 49–57.
[21]
Georlette, D.; Jonsson, Z.O.; Van Petegem, F.; Chessa, J.; Van Beeumen, J.; Hubscher, U.; Gerday, C. A DNA ligase from the psychrophile Pseudoalteromonas. haloplanktis gives insights into the adaptation of proteins to low temperatures. Eur. J. Biochem. 2000, 267, 3502–3512, doi:10.1046/j.1432-1327.2000.01377.x.
[22]
Masullo, M.; Arcari, P. Psychrophilic elongation factor TU from the Antarctic Moraxella. sp. TAC II 125: Biochemical characterization and cloning of the encoding gene. Biochemistry 2000, 39, 15531–15539, doi:10.1021/bi0018133.
[23]
Altermak, B.; Niiranen, L.; Willassen, N.P.; Smalas, A.O.; Moe, E. Comparative studies of endonuclease I from cold-adapted Vibrio. salmonicida and mesophilic Vibrio. cholerae. FEBS J. 2007, 274, 252–263, doi:10.1111/j.1742-4658.2006.05580.x.
[24]
Watanabe, S.; Yasutake, Y.; Tanaka, I.; Takada, Y. Elucidation of stability determinants of cold-adapted monomeric isocitrate dehydrogenase from a psychrophilic bazcterium, Colwellia. maris, by construction of chimeric enzymes. Microbiology 2005, 151, 1083–1094, doi:10.1099/mic.0.27667-0.
[25]
Coquelle, N.; Fioravanti, E.; Weik, M.; Vellieux, F.; Madern, D. Activity, stability and structural studies of lactate dehydrogenases adapted to extreme thermal environments. J. Mol. Biol. 2007, 374, 547–562, doi:10.1016/j.jmb.2007.09.049.
[26]
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. 2003, 185, 2161–2168, doi:10.1128/JB.185.7.2161-2168.2003.
[27]
Cartier, G.; Lorieux, F.; Allemand, F.; Dreyfus, M.; Bizebard, T. Cold adaptation in DEAD-box proteins. Biochemistry 2010, 49, 2636–2646, doi:10.1021/bi902082d.
[28]
Narinx, E.; Baise, E.; Gerday, C. Subtilisin from antarctic bacteria: Characterization and site- directed mutagenesis of residues possibly involved in the adaptation to cold. Prot. Engineer. 1997, 10, 1271–1279, doi:10.1093/protein/10.11.1271.
[29]
Alvarez, M.; Zeelen, J.P.; Mainfroid, V.; Rentier-Delrue, F.; Martial, J.A.; Wyns, L. Triose-phosphate isomerase (TIM) of the psychrophilic bacterium Vibrio. marinus. J. Biol. Chem. 1998, 273, 2199–2206.
[30]
Hochachka, P.W.; Somero, G.N. Temperature. In Biochemical Adaptation; Hochachka, P.W., Domero, G.N., Eds.; Oxford University Press: New York, NY, USA, 2002; Volume Chapter 7, p. 290.
[31]
Lonhienne, T.; Baise, E.; Feller, G.; Bouriotis, V.; Gerday, C. Enzyme activity determination on macromolecular substrates by isothermal titration calorimetry: Application to mesophilic and psychrophilic chitinases. Biochim. Biophys. Acta 2001, 1545, 349–356.
[32]
D’Amico, S.; Marx, J.-C.; Gerday, C.; Feller, G. Activity-stability relationship in extremophilic enzymes. J. Biol. Chem. 2003, 278, 7891–7896.
[33]
Suzuki, T.; Yamamoto, K.; Tada, H.; Uda, K. Cold-adapted features of arginine kinase from the deep-sea. Calyptogena. kaikoi. Mar. Biotechnol. 2012, 14, 294–303, doi:10.1007/s10126-011-9411-6.
[34]
Garsoux, G.; Lamotte-Brasseur, J.; Gerday, C.; Feller, G. Kinetic and structural optimisation to catalysis at low temperatures in a psychrophilic cellulase from the Antarctic bacterium Pseudoalteromonas. haloplanktis. Biochem. J. 2004, 384, 247–253, doi:10.1042/BJ20040325.
[35]
Lonhienne, T.; Zoidakis, J.; Vorgias, E.; Feller, G.; Gerday, C.; Bouriotis, V. Modular structure, local flexibility and cold-activity of a novel chitobiase from a psychrophilic Antarctic bacterium. J. Mol. Biol. 2001, 310, 291–297, doi:10.1006/jmbi.2001.4774.
[36]
Sotelo-Mundo, R.R.; Lopez-Zavala, A.A.; Garcia-Orozco, K.D.; Arvizu-Flores, A.A.; Velazquez-Conteras, E.F.; Vaalenzuela-Soto, E.M.; Rojo-Dominguez, A.; Kanost, M.R. The lysozyme from insect (Manduca. sexta) is a cold-adapted enzyme. Protein Pept. Lett. 2007, 14, 774–778, doi:10.2174/092986607781483688.
[37]
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. 1994, 269, 17448–17453.
[38]
Collins, T.; Meuwis M-A. Gerday, C.; Feller, G. Activity, stability and flexibility in glycosidases adapted to extreme thermal environments. J. Mol. Biol. 2003, 328, 419–428, doi:10.1016/S0022-2836(03)00287-0.
[39]
Petrescu, J.; Lamotte-Brasseur, J.; Chessa, J.-P.; Ntarima, P.; Claeyssens, M.; Devreese, B.; Marino, G.; Gerday, C. Xylanase from psychrophilic yeast Cryptococcus. adeliae. Extremophiles 2000, 4, 137–144, doi:10.1007/s007920070028.
[40]
Marx, J.-C.; Collins, S.; D’Amico, S.; Feller, G.; Gerday, C. Cold-adapted enzymes from marine Antarctic microorganisms. Mar. Biotechnol. 2006, 9, 293–304.
[41]
Robindon, G.W.; Cho, C.H. Role of hydration water in protein unfolding. Biophys. J. 1999, 77, 3331–3318.
[42]
Loladze, V.V.; Ermolenko, D.N.; Makhatadze, G.I. Heat capacity changes upon burial of polar and non polar groups in proteins. Protein Sci. 2001, 10, 1343–1352.
[43]
Kumar, S.; Tsai, C.J.; Nussinov, R. Maximal stabilities of reversible two-state proteins. Biochemistry. 2002, 41, 5359–5374, doi:10.1021/bi012154c.
[44]
Feller, G. Protein stability and enzyme activity at extreme biological temperatures. J. Phys. Condens. Matter 2010, 22, 32–49, doi:10.1088/0953-8984/22/32/323101.
[45]
Chakravarty, S.; Varadarajan, R. Elucidation of factors responsible for enhanced thermal stabilitiy of protein: A structural genomics based study. Biochemistry 2002, 41, 8152–8161, doi:10.1021/bi025523t.
[46]
D’Amico, S.; Gerday, C.; Feller, G. Dual effects of an extra disulfide bond on the activity and stability of a cold-adapted α-amylase. J. Biol. Chem. 2002, 277, 46110–46115, doi:10.1074/jbc.M207253200.
[47]
Cipolla, A.; D’Amico, S.; Barumandzadeh, R.; Matagne, A.; Feller, G. Stepwise adaptations to low temperature as revealed by multiple muatnts of psychrophilic α-amylase from Antarctic bacterium. J. Biol. Chem. 2011, 286, 38348–38555.
[48]
Papaleo, E.; Pasi, M.; Tiberti, M.; De Gioia, L. Molecular dynamics of mesophilic-like mutants of a cold-adapted enzyme: Insights into distal effects induced by the mutations. PLoS One 2011, 6, e24214.
[49]
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. 2000, 297, 1015–1026, doi:10.1006/jmbi.2000.3612.
[50]
Taguchi, S.; Komada, S.; Momose, H. The complete amino acid substitutions at position 131 that are positively involved in cold adaptation of subtilisin BPN’. Appl. Environ. Microbiol. 2000, 66, 1410–1415, doi:10.1128/AEM.66.4.1410-1415.2000.
[51]
Zong, C.Q.; Song, S.; Fang, N.; Liang, X.; Zhu, H.; Tang, X.; Tang, B. Improvement of low-temperature caseinolytic activity of a thermophilic subtilase by directed evolution and site-directed mutagenesis. Biotechnol. Bioeng. 2009, 104, 862–870, doi:10.1002/bit.22473.
[52]
Bae, E.; Phillips, G.N. Structure and analysis of highly homologous psychrophilic, mesophilic and thermophilic adenylate kinases. J. Biol. Chem. 2004, 279, 28202–28208, doi:10.1074/jbc.M401865200.
[53]
Davlieva, M.; Shammo, Y. Structure and biochemical characterization of an adenylate kinase originating from the psychrophilic organism Marinibacillus. marinus. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2009, 65, 751–756, doi:10.1107/S1744309109024348.
[54]
Aghajari, N.; Van Petegem, F.; Villeret, V.; Chessa, J.P.; Gerday, C.; Haser, R.; Van Beeumen, J. Crystal structures of a psychrophilic metalloprotease reveal new insights into catalysis by cold-adapted proteases. Proteins 2003, 50, 636–647, doi:10.1002/prot.10264.
[55]
De Baker, M.; McSweeney, S.; Rasmussen, H.B.; Riise, B.W.; Lindley, P.; Hough, E. 9 ？ crystal structure of heat-labile shrimp alkaline phosphatase. J. Mol. Biol. 2002, 318, 1265–1274, doi:10.1016/S0022-2836(02)00035-9.
[56]
Wang, E.; Koutsioulis, D.; Leiros, H.K.; Andersen, O.A.; Bouriotis, V.; Hough, E.; Heikinheimo, P. Crystal structure of alkaline phosphatase from the Antarctic bacterium TAB5. J. Mol. Biol. 2007, 366, 1318–1331, doi:10.1016/j.jmb.2006.11.079.
[57]
Helland, R.; Leiros, I.; Berglund, G.I.; Willassen, N.P.; Smalas, A.O. The crystral structure of anionic salmon trypsin in complex with bovine pancreatic trypsin inhibitor. Eur. J. Biochem. 1998, 256, 317–324.
[58]
Aghajari, N.; Feller, G.; Gerday, C.; Haser, R. Structures of the psychrophilic Alteromonas. haloplanctis alpha-amylase give insights into cold adaptation at a molecular level. Structure 1998, 6, 1503–1516, doi:10.1016/S0969-2126(98)00149-X.
[59]
De Vos, D.; Xu, Y.; Hulpiau, P.; Vergauwen, B.; Van Beeumen, J.J. Structural investigation of cold activity and regulation of aspartate carbamoyltransferase from the extreme psychrophilic bacterium Moritella. profunda. J. Mol. Biol. 2007, 365, 379–395, doi:10.1016/j.jmb.2006.09.064.
[60]
Skalova, T.; Dohnalek, J.; Spiwok, V.; Lipovova, P.; Vondrackova, E.; Petrokova, H.; Duskova, J.; Strnad, H.; Kralova, B.; Hasek, J. Cold-active beta-galactosidase from Arthrobacter. sp. C2–2 forms compact 660 kDa hexamers: Crystal structure at 1.9 ？ resolution. J. Mol. Biol. 2005, 353, 282–294, doi:10.1016/j.jmb.2005.08.028.
[61]
Riise, E.K.; Lorentzen, M.S.; Helland, R.; Smalas, A.O.; Leiros, H.-K.S.; Willassen, N.P. The first structure of a cold-active catalase from Vibrio. salmo nicida at 1.96 ？ reveals structural aspects of cold adaptation. Acta Crystallogr. D Biol. Crystallogr. 2007, 63, 135–148.
[62]
Violot, S.; Aghajari, N.; Czjzek, M.; Feller, G.; Sonan, G.; Gouet, P.; Gerday, C.; Haser, R.; Receveur-Bréchot, V. Structure of a full length psychrophilic cellulase from Pseudoalteromonas. haloplanktis revealed by X-ray diffraction and small angle X-ray scattering. J. Mol. Biol. 2005, 348, 1211–1224, doi:10.1016/j.jmb.2005.03.026.
[63]
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 1998, 6, 351–361, doi:10.1016/S0969-2126(98)00037-9.
[64]
Berglund, G.I.; Willassen, N.P.; Hordvik, A.; Smalas, A.O. Structure of native pancreatic elastase from North Atlantic salmon at 1.61 ？ resolution. Acta Crystallogr. D Biol. Crystallogr. 1995, 51, 925–937, doi:10.1107/S0907444995004835.
[65]
Brzuszkiewicz, A.; Nowak, E.; Dauter, Z.; Dauter, M.; Cieslinski, H.; Dlugolecka, A.; Kur, J. Structure of EstA esterase from psychrotrophic Pseudoalteromonas. sp. 643A covanently inhibited by monoethylphosphonate. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2009, 65, 862–865, doi:10.1107/S1744309109030826.
[66]
Uppenberg, J.; Hansen, M.T.; Paktar, S.; Jones, T.A. The sequence, crystal structure determination and refinement of two crystal forms of lipase B from Candida antarctica. Structure 1994, 2, 293–308, doi:10.1016/S0969-2126(00)00031-9.
[67]
Kim, S.Y.; Hwang, K.Y.; Kim, S.H.; Sung, H.C.; Han, Y.S.; Cho, Y. Structural basis for cold adaptation. Sequence, biochemical properties, and crystal structure of malate dehydrogenase from a psychrophile Aquaspirillium. arcticum. J. Biol. Chem. 1999, 274, 11761–11767.
[68]
Karlsen, S.; Hough, E.; Olsen, R.L. Structure and proposed amino-acid sequence of a trypsin from Atlantic cod (Gadus. morhua). Acta Crystallogr. D Biol. Crystallogr. 1998, 54, 32–46, doi:10.1107/S090744499700810X.
[69]
Leiros, H.K.; Pey, A.L.; Innselset, M.; Moe, E.; Leiros, I.; Steen, I.H.; Martinez, A. Structure of phenylalanine hydroxylase from Colwellia. psychrerythraea 34H, a monomeric cold active enzyme with local flexibility around the active site and high overall stability. J. Biol. Chem. 1997, 282, 21973–21986.
[70]
Helland, R.; Larsen, A.N.; Smalas, A.O.; Willassen, N.P. ？ crystal structure of a proteinase K-like enzyme from a psychrotroph Serratia. species. FEBS. J. 2006, 273, 61–71, doi:10.1111/j.1742-4658.2005.05040.x.
[71]
Tsuruta, H.; Mikami, B.; Aizono, Y. Crystal structure of cold-active protein-tyrosine phosphatase from a psychrophile, Shewanella. sp. J. Biochem. 2005, 137, 69–77, doi:10.1093/jb/mvi010.
[72]
Alterio, V.; Aurilia, V.; Romanelli, A.; Parracino, A.; Saviano, M.; D’Auria, S.; De Simone, G. Crystal structure of an S-formyl glutathione hydrolase from Pseudoalteromonas. haloplanktis TAC 125. Biopolymers 2010, 93, 669–677.
[73]
Arnorsdottir, J.; Kristjansson, M.M.; Ficner, R. Crystal structure of a subtilisin-like serine proteinase from a psychrotrophic Vibrio. species reveals structural aspects of cold adaptation. FEBS. J. 2005, 272, 832–845, doi:10.1111/j.1742-4658.2005.04523.x.
[74]
Almog, O.; Gonzalez, A.; Godin, N.; de Leeuw, M.; Mekel, M.J.; Klein, D.; Braun, S.; Shoham, G.; Walter, R.L. The crystal structure of the psychrophilic subtilisin S41 and the mesophilic subtilisin Sph reveal the same calcium-loaded state. Proteins 2009, 74, 489–496, doi:10.1002/prot.22175.
[75]
Pedersen, H.L.; Willassen, N.P.; Leiros, I. The first structure of a cold-adapted superoxide dismutase (SOD): Biochemical and structural characterization of iron SOD from Aliivibrio. samonicida. Acta Crystallogr. Sect. F Biol. Cryst. Commun. 2009, 65, 84–92, doi:10.1107/S1744309109001110.
[76]
Toyota, E.; Ng, K.K.; Kuninaga, S.; Sekizaki, H.; Itoh, K.; Tanizawa, K.; James, M.N. Crystal structure and nucleotide sequence of an anionic trypsin from chum salmon (Oncorrhynchus. keta) in comparison with Atlantic salmon (Salmo. salar) and bovine trypsin. J. Mol. Biol. 2002, 324, 391–397, doi:10.1016/S0022-2836(02)01097-5.
[77]
Leiros, I.; Moe, E.; Lanes, O.; Smalas, A.O.; Willassen, N.P. The structure of uracil-DNA glycosylase from Atlantic cod (Gadus. morhua) reveals cold-adaptation features. Acta Crystallogr. D Biol. Crystallogr. 2003, 59, 1357–1365, doi:10.1107/S0907444903011144.
[78]
Van Petegem, F.; Collins, T.; Meuwis, M.A.; Gerday, C.; Feller, G.; Van Beeumen, J. The structure of a cold-adapted family 8 xylanase at 1.3 ？ resolution. Structural adaptations to cold and investigation of the active site. J. Biol. Chem. 2003, 278, 7531–7539.
[79]
Hoffman, A.; Bukau, B.; Kramer, G. Structure and function of the molecular chaperone, trigger factor. Biophys. Biochim. Acta 2010, 1803, 650–661.
[80]
Tartaglia, G.G.; Dobson, C.M.; Hartl, F.U. Physicochemical determinants of chaperone requirements. J. Mol. Biol. 2010, 400, 579–588, doi:10.1016/j.jmb.2010.03.066.
[81]
N？lting, B.; Salimi, N.; Guth, U. Protein folding forces. J. Theor. Biol. 2008, 251, 331–347, doi:10.1016/j.jtbi.2007.11.020.
[82]
Gianni, S.; Ivarsson, Y.; Jemth, P.; Brunori, M.; Travaglini-Allocatelli, C. Identification and characterization of protein folding intermediates. Biophys. Chem. 2007, 128, 105–113, doi:10.1016/j.bpc.2007.04.008.
[83]
Xie, B.; Bian, F.; Chen, X.; He, H.; Guo, J.; Gao, X.; Zeng, Y.; Chen, B.; Zhou, B.; Zhang, Y. Cold adaptation of zinc metalloprotease in the thermolysin family from deep sea and Arctic sea ice bacteria revealed by catalytic and structural properties and molecular dynamics. J. Biol. Chem. 2009, 284, 9257–9269.
[84]
Mereghetti, P.; Riccardi, L.; Brandsdal, B.O.; Fantucci, P.; De Gioia, L.; Papaleo, E. Near native-state conformational landscape of psychrophilic and mesophilic enzymes: Probing the folding funnel model. J. Phys. Chem. B. 2010, 114, 7609–7619.
[85]
Ferrer, M.; Chernikova, T.N.; Yakimov, M.M.; Golyshin, P.N.; Timmis, K.N. Chaperonins govern growth of Escherichia coli at low temperatures. Nat. Biotechnol. 2003, 21, 1266–1267, doi:10.1038/nbt1103-1266.
[86]
Ferrer, M.; Lunsdorf, H.; Chernikova, T.N.; Yakimov, M.; Timmis, K.N.; Golyshin, P.N. Functional consequences of single: Double ring transitions in chaperonins: Life in the cold. Mol. Microbiol. 2004, 53, 167–182, doi:10.1111/j.1365-2958.2004.04077.x.
[87]
Goodchild, A.; Saunders, N.F.; Erlan, H.; Raftery, M.; Guilhaus, M.; Curmi, P.M.; Cavicchioli, R. A Proteomic determination of cold-adaptation in the Antarctic archaeon, Methanococcoides. burtonii. Mol. Microbiol. 2004, 53, 309–321, doi:10.1111/j.1365-2958.2004.04130.x.
[88]
Piette, F.; D’Amico, S.; Struvay, C.; Mazzuchelli, G.; Renaut, J.; Tutino, M.L.; Danchin, A.; Leprince, P.; Feller, G. Proteomics of life of low temperatures: Trigger factor is the primary chaperone in the Antarctic bacterium Pseudoalteromonas. haloplanktis TAC 125. Mol. Microbiol. 2010, 76, 120–132, doi:10.1111/j.1365-2958.2010.07084.x.
[89]
Ting, L.; Williams, T.J.; Cowley, M.J.; Lauro, F.M.; Guilhaus, M.; Raftery, M.J.; Cavicchioli, R. Cold adaptation in the marine bacterium Sphingopyxis. alaskensis assessed using quantitative proteomics. Environ. Microbiol. 2010, 12, 2658–2676.
[90]
Mykytczuk, N.C.; Trevors, J.T.; Foote, S.J.; Leduc, L.G.; Ferroni, G.D.; Twine, S.M. Proteomics insights into cold adaptation of psychrotrophic and mesophilic Acidothiobacillus. ferrooxidans strains. Van Leeuwenhoek 2011, 100, 259–277, doi:10.1007/s10482-011-9584-z.
[91]
Kandror, O.; Goldberg, A.L. Trigger factor is induced upon cold shock and enhances viability of Escherichia coli at low temperatures. Proc. Natl. Acad. Sci. USA 1997, 94, 4978–4981, doi:10.1073/pnas.94.10.4978.
[92]
Kramer, G.; Patzelt, H.; Rauch, T.; Kurtz, T.A.; Vorderwulbecke, S.; Bukau, B.; Deurling, E. Trigger factor peptidyl-prolyl cis/trans isomerase activity is not essential for the folding of cytosolic proteins in Escherichia coli. J. Biol. Chem. 2004, 14, 14165–14170.
