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Psychrophilic Enzymes: Cool Responses to Chilly Problems

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Extremophiles Handbook

Introduction

Most of the biotopes on Earth are permanently exposed to low temperatures. This includes the Antarctic continent, the Arctic ice floe, the permafrost, the mountain and glacier regions, and the deep-sea waters, the latter covering 70% of the planet surface. If a psychrophile is defined as an organism living permanently at temperatures close to the freezing point of water, in thermal equilibrium with the medium, this definition encompasses a large range of species from Bacteria, Archaea, and Eukaryotes. This aspect underlines that psychrophiles are numerous, taxonomically diverse, and have a widespread distribution. In these organisms, low temperatures are essential for sustained cell metabolism. Some psychrophilic bacteria grown at 4°C have doubling times close to that of Escherichia coliat 37°C. Such deep adaptation of course requires a vast array of metabolic and structural adjustments at nearly all organization levels of the cell, which begins to be understood thanks...

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References

  • Aghajari N, Feller G, Gerday C, Haser R (1998a) Crystal structures of the psychrophilic α-amylase from Alteromonas haloplanctis in its native form and complexed with an inhibitor. Protein Sci 7:564–572

    Article  PubMed  CAS  Google Scholar 

  • Aghajari N, Feller G, Gerday C, Haser R (1998b) Structures of the psychrophilic Alteromonas haloplanctis α-amylase give insights into cold adaptation at a molecular level. Structure 6:1503–1516

    Article  PubMed  CAS  Google Scholar 

  • Aghajari N, Roth M, Haser R (2002) Crystallographic evidence of a transglycosylation reaction: ternary complexes of a psychrophilic alpha-amylase. Biochemistry 41:4273–4280

    Article  PubMed  CAS  Google Scholar 

  • Aghajari N, Van Petegem F, Villeret V, Chessa JP, Gerday C, Haser R, Van Beeumen J (2003) Crystal structures of a psychrophilic metalloprotease reveal new insights into catalysis by cold-adapted proteases. Proteins 50:636–647

    Article  PubMed  CAS  Google Scholar 

  • Bae E, Phillips GN Jr (2004) Structures and analysis of highly homologous psychrophilic, mesophilic, and thermophilic adenylate kinases. J Biol Chem 279:28202–28208

    Article  PubMed  CAS  Google Scholar 

  • Bae E, Phillips GN Jr (2006) Roles of static and dynamic domains in stability and catalysis of adenylate kinase. Proc Natl Acad Sci USA 103:2132–2137

    Article  PubMed  CAS  Google Scholar 

  • Bell GS, Russell RJ, Connaris H, Hough DW, Danson MJ, Taylor GL (2002) Stepwise adaptations of citrate synthase to survival at life’s extremes. From psychrophile to hyperthermophile. Eur J Biochem 269:6250–6260

    Article  PubMed  CAS  Google Scholar 

  • Benkovic SJ, Hammes GG, Hammes-Schiffer S (2008) Free-energy landscape of enzyme catalysis. Biochemistry 47:3317–3321

    Article  PubMed  CAS  Google Scholar 

  • Bjelic S, Brandsdal BO, Aqvist J (2008) Cold adaptation of enzyme reaction rates. Biochemistry 47:10049–10057

    Article  PubMed  CAS  Google Scholar 

  • Brandsdal BO, Smalas AO, Aqvist J (2001) Electrostatic effects play a central role in cold adaptation of trypsin. FEBS Lett 499:171–175

    Article  PubMed  CAS  Google Scholar 

  • Casanueva A, Tuffin M, Cary C, Cowan DA (2010) Molecular adaptations to psychrophily: the impact of ‘omic’ technologies. Trends Microbiol 18:374–381

    Article  PubMed  CAS  Google Scholar 

  • Cherry JR, Lamsa MH, Schneider P, Vind J, Svendsen A, Jones A, Pedersen AH (1999) Directed evolution of a fungal peroxidase. Nat Biotechnol 17:379–384

    Article  PubMed  CAS  Google Scholar 

  • Chiuri R, Maiorano G, Rizzello A, del Mercato LL, Cingolani R, Rinaldi R, Maffia M, Pompa PP (2009) Exploring local flexibility/rigidity in psychrophilic and mesophilic carbonic anhydrases. Biophys J 96:1586–1596

    Article  PubMed  CAS  Google Scholar 

  • Claverie P, Vigano C, Ruysschaert JM, Gerday C, Feller G (2003) The precursor of a psychrophilic alpha-amylase: structural characterization and insights into cold adaptation. Biochim Biophys Acta 1649: 119–122

    Article  PubMed  CAS  Google Scholar 

  • Collins T, Meuwis MA, Gerday C, Feller G (2003) Activity, stability and flexibility in glycosidases adapted to extreme thermal environments. J Mol Biol 328:419–428

    Article  PubMed  CAS  Google Scholar 

  • D’Amico S, Gerday C, Feller G (2001) Structural determinants of cold adaptation and stability in a large protein. J Biol Chem 276:25791–25796

    Article  PubMed  Google Scholar 

  • D’Amico S, Claverie P, Collins T, Georlette D, Gratia E, Hoyoux A, Meuwis MA, Feller G, Gerday C (2002a) Molecular basis of cold adaptation. Philos Trans R Soc Lond B Biol Sci 357:917–925

    Article  PubMed  Google Scholar 

  • D’Amico S, Gerday C, Feller G (2002b) Dual effects of an extra disulfide bond on the activity and stability of a cold-adapted alpha-amylase. J Biol Chem 277:46110–46115

    Article  PubMed  Google Scholar 

  • D’Amico S, Gerday C, Feller G (2003a) Temperature adaptation of proteins: engineering mesophilic-like activity and stability in a cold-adapted alpha-amylase. J Mol Biol 332:981–988

    Article  PubMed  Google Scholar 

  • D’Amico S, Marx JC, Gerday C, Feller G (2003b) Activity-stability relationships in extremophilic enzymes. J Biol Chem 278:7891–7896

    Article  PubMed  Google Scholar 

  • D’Amico S, Collins T, Marx JC, Feller G, Gerday C (2006a) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389

    Article  PubMed  Google Scholar 

  • D’Amico S, Sohier JS, Feller G (2006b) Kinetics and energetics of ligand binding determined by microcalorimetry: insights into active site mobility in a psychrophilic alpha-amylase. J Mol Biol 358:1296–1304

    Article  PubMed  Google Scholar 

  • De Vos D, Collins T, Nerinckx W, Savvides SN, Claeyssens M, Gerday C, Feller G, Van Beeumen J (2006) Oligosaccharide binding in family 8 glycosidases: crystal structures of active-site mutants of the beta-1, 4-xylanase pXyl from Pseudoaltermonas haloplanktis TAH3a in complex with substrate and product. Biochemistry 45:4797–4807

    Article  PubMed  CAS  Google Scholar 

  • Dinner AR, Sali A, Smith LJ, Dobson CM, Karplus M (2000) Understanding protein folding via free-energy surfaces from theory and experiment. Trends Biochem Sci 25:331–339

    Article  PubMed  CAS  Google Scholar 

  • Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1:200–208

    Article  PubMed  CAS  Google Scholar 

  • Feller G, D’Amico D, Gerday C (1999) Thermodynamic stability of a cold-active α-amylase from the Antarctic bacterium Alteromonas haloplanctis. Biochemistry 38:4613–4619

    Article  PubMed  CAS  Google Scholar 

  • Fields PA, Somero GN (1998) 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

    Article  PubMed  CAS  Google Scholar 

  • Garsoux G, Lamotte J, Gerday C, Feller G (2004) Kinetic and structural optimization to catalysis at low temperatures in a psychrophilic cellulase from the Antarctic bacterium Pseudoalteromonas haloplanktis. Biochem J 384:247–253

    Article  PubMed  CAS  Google Scholar 

  • Georlette D, Damien B, Blaise V, Depiereux E, Uversky VN, Gerday C, Feller G (2003) Structural and functional adaptations to extreme temperatures in psychrophilic, mesophilic, and thermophilic DNA ligases. J Biol Chem 278:37015–37023

    Article  PubMed  CAS  Google Scholar 

  • Gerday C, Glansdorff N (2007) Physiology and biochemistry of extremophiles. ASM Press, Washington

    Google Scholar 

  • Gianese G, Bossa F, Pascarella S (2002) Comparative structural analysis of psychrophilic and meso- and thermophilic enzymes. Proteins 47:236–249

    Article  PubMed  CAS  Google Scholar 

  • Giver L, Gershenson A, Freskgard PO, Arnold FH (1998) Directed evolution of a thermostable esterase. Proc Natl Acad Sci USA 95:12809–12813

    Article  PubMed  CAS  Google Scholar 

  • Gorfe AA, Brandsdal BO, Leiros HK, Helland R, Smalas AO (2000) Electrostatics of mesophilic and psychrophilic trypsin isoenzymes: qualitative evaluation of electrostatic differences at the substrate binding site. Proteins 40:207–217

    Article  PubMed  CAS  Google Scholar 

  • Kim SY, Hwang KY, Kim SH, Sung HC, Han YS, Cho YJ (1999) 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

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Nussinov R (2004) Experiment-guided thermodynamic simulations on reversible two-state proteins: implications for protein thermostability. Biophys Chem 111:235–246

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Ma B, Tsai CJ, Sinha N, Nussinov R (2000) Folding and binding cascades: dynamic landscapes and population shifts. Protein Sci 9:10–19

    Article  PubMed  CAS  Google Scholar 

  • Leiros I, Moe E, Lanes O, Smalas AO, Willassen NP (2003) The structure of uracil-DNA glycosylase from Atlantic cod (Gadus morhua) reveals cold-adaptation features. Acta Crystallogr D Biol Crystallogr 59:1357–1365

    Article  PubMed  Google Scholar 

  • Lonhienne T, Gerday C, Feller G (2000) Psychrophilic enzymes: revisiting the thermodynamic parameters of activation may explain local flexibility. Biochim Biophys Acta 1543:1–10

    Article  PubMed  CAS  Google Scholar 

  • Lonhienne T, Zoidakis J, Vorgias CE, Feller G, Gerday C, Bouriotis V (2001) Modular structure, local flexibility and cold-activity of a novel chitobiase from a psychrophilic Antarctic bacterium. J Mol Biol 310:291–297

    Article  PubMed  CAS  Google Scholar 

  • Ma B, Kumar S, Tsai CJ, Hu Z, Nussinov R (2000) Transition-state ensemble in enzyme catalysis: possibility, reality, or necessity? J Theor Biol 203:383–397

    Article  PubMed  CAS  Google Scholar 

  • Makhatadze GI, Privalov PL (1995) Energetics of protein structure. Adv Protein Chem 47:307–425

    Article  PubMed  CAS  Google Scholar 

  • Mandrich L, Pezzullo M, Del Vecchio P, Barone G, Rossi M, Manco G (2004) Analysis of thermal adaptation in the HSL enzyme family. J Mol Biol 335:357–369

    Article  PubMed  CAS  Google Scholar 

  • Margesin R, Schinner F, Marx JC, Gerday C (2008) Psychrophiles, from biodiversity to biotechnology. Springer, Berlin/Heidelberg

    Book  Google Scholar 

  • Privalov PL (1990) Cold denaturation of proteins. Crit Rev Biochem Mol Biol 25:281–305

    Article  PubMed  CAS  Google Scholar 

  • Qian M, Haser R, Buisson G, Duee E, Payan F (1994) The active center of a mammalian alpha-amylase. Structure of the complex of a pancreatic alpha-amylase with a carbohydrate inhibitor refined to 2.2-Å resolution. Biochemistry 33:6284–6294

    Article  PubMed  CAS  Google Scholar 

  • Russell NJ (2000) Toward a molecular understanding of cold activity of enzymes from psychrophiles. Extremophiles 4:83–90

    Article  PubMed  CAS  Google Scholar 

  • Russell RJ, Gerike U, Danson MJ, Hough DW, Taylor GL (1998) Structural adaptations of the cold-active citrate synthase from an Antarctic bacterium. Structure 6:351–361

    Article  PubMed  CAS  Google Scholar 

  • Schultz CP (2000) Illuminating folding intermediates. Nat Struct Biol 7:7–10

    Article  PubMed  CAS  Google Scholar 

  • Siddiqui KS, Cavicchioli R (2006) Cold-adapted enzymes. Annu Rev Biochem 75:403–433

    Article  PubMed  CAS  Google Scholar 

  • Siddiqui KS, Feller G, D’Amico S, Gerday C, Giaquinto L, Cavicchioli R (2005) The active site is the least stable structure in the unfolding pathway of a multidomain cold-adapted alpha-amylase. J Bacteriol 187:6197–6205

    Article  PubMed  CAS  Google Scholar 

  • Skalova T, Dohnalek J, Spiwok V, Lipovova P, Vondrackova E, Petrokova H, Duskova J, Strnad H, Kralova B, Hasek J (2005) Cold-active beta-galactosidase from Arthrobacter sp. C2-2 forms compact 660 kDa hexamers: crystal structure at 1.9Å resolution. J Mol Biol 353:282–294

    Article  PubMed  CAS  Google Scholar 

  • Smalas AO, Leiros HK, Os V, Willassen NP (2000) Cold adapted enzymes. Biotechnol Annu Rev 6:1–57

    Article  PubMed  CAS  Google Scholar 

  • Somero GN (1995) Proteins and temperature. Annu Rev Physiol 57:43–68

    Article  PubMed  CAS  Google Scholar 

  • Suzuki Y, Takano K, Kanaya S (2005) Stabilities and activities of the N- and C-domains of FKBP22 from a psychrotrophic bacterium overproduced in Escherichia coli. FEBS J 272:632–642

    Article  PubMed  CAS  Google Scholar 

  • Tehei M, Franzetti B, Madern D, Ginzburg M, Ginzburg BZ, Giudici-Orticoni MT, Bruschi M, Zaccai G (2004) Adaptation to extreme environments: macromolecular dynamics in bacteria compared in vivo by neutron scattering. EMBO Rep 5:66–70

    Article  PubMed  CAS  Google Scholar 

  • Tsai CJ, Ma B, Nussinov R (1999) Folding and binding cascades: shifts in energy landscapes. Proc Natl Acad Sci USA 96:9970–9972

    Article  PubMed  CAS  Google Scholar 

  • Tsigos I, Velonia K, Smonou I, Bouriotis V (1998) Purification and characterization of an alcohol dehydrogenase from the Antarctic psychrophile Moraxella sp. TAE123. Eur J Biochem 254:356–362

    Article  PubMed  CAS  Google Scholar 

  • Vetriani C, Maeder DL, Tolliday N, Yip KS, Stillman TJ, Britton KL, Rice DW, Klump HH, Robb FT (1998) Protein thermostability above 100°C: a key role for ionic interactions. Proc Natl Acad Sci USA 95:12300–12305

    Article  PubMed  CAS  Google Scholar 

  • Violot S, Aghajari N, Czjzek M, Feller G, Sonan GK, Gouet P, Gerday C, Haser R, Receveur-Brechot V (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 348:1211–1224

    Article  PubMed  CAS  Google Scholar 

  • Wintrode PL, Arnold FH (2000) Temperature adaptation of enzymes: lessons from laboratory evolution. Adv Protein Chem 55:161–225

    Article  PubMed  CAS  Google Scholar 

  • Xie BB, Bian F, Chen XL, He HL, Guo J, Gao X, Zeng YX, Chen B, Zhou BC, Zhang YZ (2009) Cold adaptation of zinc metalloproteases in the thermolysin family from deep sea and arctic sea ice bacteria revealed by catalytic and structural properties and molecular dynamics: new insights into relationship between conformational flexibility and hydrogen bonding. J Biol Chem 284:9257–9269

    Article  PubMed  CAS  Google Scholar 

  • Xu Y, Feller G, Gerday C, Glansdorff N (2003) Metabolic enzymes from psychrophilic bacteria: challenge of adaptation to low temperatures in ornithine carbamoyltransferase from Moritella abyssi. J Bacteriol 185:2161–2168

    Article  PubMed  CAS  Google Scholar 

  • Yip KS, Stillman TJ, Britton KL, Artymiuk PJ, Baker PJ, Sedelnikova SE, Engel PC, Pasquo A, Chiaraluce R, Consalvi V (1995) The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion-pair networks in maintaining enzyme stability at extreme temperatures. Structure 3:1147–1158

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Research at the author’s laboratory was supported by the European Union, the Région wallonne (Belgium), the Fonds National de la Recherche Scientifique (Belgium), and the University of Liège. The facilities offered by the Institut Polaire Français are also acknowledged.

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Authors and Affiliations

  1. Laboratory of Biochemistry, Center for Protein Engineering, Institute of Chemistry B6, University of Liège, B-4000, Liège-Sart Tilman, Belgium

    Frédéric Roulling, Florence Piette, Alexandre Cipolla, Caroline Struvay & Dr. Georges Feller

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  1. Frédéric Roulling
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  2. Florence Piette
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  3. Alexandre Cipolla
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  4. Caroline Struvay
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  5. Dr. Georges Feller
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Correspondence to Georges Feller .

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  1. Extremobiosphere Research Center, Japan Agency for Marine-Earth Science and Technology (JAMSTEC) Yokohama, Professor Emeritus of Tokyo Institute of Technology, Tokyo, Japan

    Koki Horikoshi

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Roulling, F., Piette, F., Cipolla, A., Struvay, C., Feller, G. (2011). Psychrophilic Enzymes: Cool Responses to Chilly Problems. In: Horikoshi, K. (eds) Extremophiles Handbook. Springer, Tokyo. https://doi.org/10.1007/978-4-431-53898-1_43

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