Abstract
Cold-active enzymes are produced by organisms, known as psychrophiles, adapted to permanently cold habitats. Low temperatures have an exponential deleterious effct on reaction rates, and thus psychrophilic enzymes have to be adapted to secure appropriate reaction rates in their environment. These enzymes have a high specific activity at low temperatures, in any case higher than that of their mesophilic and thermophilic counterparts, and display a shift of the apparent optimum temperature for activity towards low temperatures as well as a reduced thermal stability and increased flexibility. The increased flexibility may be global, involving the overall edifice, or local, involving only those zones crucial for activity, be they near or distant from the active site. The reduced thermodynamic stability of cold-adapted enzymes is illustrated by a significantly lower stabilisation energy as compared to that of their mesophilic and thermophilic counterparts, yet maximum stability occurs at similar temperatures in all cases. The comparison of their three-dimensional structures with higher temperature-adapted homologues, in conjunction with various mutagenesis studies, has shown that their high activity results from rather discrete molecular changes that tend to decrease the stability of the molecular edifice. Each cold-adapted enzyme however adopts a specific strategy. There is apparently a continuum in the adaptation, with some enzymes showing extremely acute cold adaptation, as illustrated by a severe shift of the activity towards low temperatures, whereas others appear to cover a broader range of temperatures. This probably depends on the specific evolutionary history of the organisms which produce them.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adekoya OA, Helland R, Willassen NP, Sylte I (2006) Comparative sequence and structure analysis reveal features of cold adaptation of an enzyme in the thermolysin family. Proteins 62:435–439
Aghajari N, Feller G, Gerday C, Haser R (1998) Structures of the psychrophilic Alteromonas haloplanktis α-amylase give insights into cold adaptation at a molecular level. Structure 6:1503–1516
Almog O, Gonzalez A, Godin N, de Leeuw M, Mekel MJ, Klein D, Braun S, Shoham G, Walter RL (2009) The crystal structure of the psychrophilic subtilisin S41 and the mesophilic subtilisin Sph reveal the same calcium loaded state. Proteins 74:489–496
Altermark B, Niiranen L, Willassen NP, Smalas AO, Moe E (2007) Comparative studies of endonuclease I from cold-adapted Vibrio salmonicida and mesophilic Vibrio cholerae. FEBS J 274:252–263
Angelaccio S, Florio R, Consalvi V, Festa G, Pascarella P (2012) Serine hydroxymethyltransferase from the cold-adapted microorganism Psychromonas ingrahamii: a low temperature active enzyme with broad specificity. Int J Mol Sci 13:1314–1326
Arcus VL, Prentice EJ, Hobbs JK, Mulholland AJ, Van der Kamp MW, Pudney CR, Parker EJ, Schipper LA (2016) On the temperature dependence of enzyme-catalysed rates. Biochemistry 55:1681–1688
Arnorsdóttir J, Helgadóttir S, Thorbjarnardóttir SH, Eggertsson G, Kristjansson MM (2007) Effect of selected Ser/Ala and Xaa/Pro mutations on the stability and catalytic properties of a cold adapted subtilisin-like serine proteinase. Biochim Biophys Acta 1774:749–755
Arrhenius S (1889) Uber die Reaktionsgeschwindigkeit bei der Inversion von Rohrzuckerdurch Säuren. Z Physic Chem 4:226–248
Asgeirsson B, Adalbjörsson BV, Gylfason GA (2007) Engineered disulfide bonds increase active-site local stability and reduce catalytic activity of a cold-adapted alkaline phosphatase. Biochim Biophys Acta 1774:679–687
Berg TO, Gurung MK, Altermark B, Smalas AO, Raeder H (2015) Characterization of the N-acetylneuraminic acid synthase (NeuB) from the psychrophilic fish pathogen Moritella viscosa. Carbohydr Res 402:133–145
Bjelic S, Bransdal BO, Aqvist J (2008) Cold adaptation of enzyme reaction rates. Biochemistry 47:10049–10057
Budiman C, Koga Y, Takano K, Kanaya S (2011) FK 506-binding protein 22 from a psychrophilic bacterium, a cold shock-inducible peptidyl prolyl isomerase with the ability to assist in protein folding. Int J Mol Sci 12:5261–5284
Chess JP, Petrescu I, Bentahir M, Van Beeumen J, Gerday C (2000) Purification, physico-chemical characterization and sequence of the heat-labile alkaline metalloprotease from a psychrophilic Pseudomonas species. Biochim Biophys Acta 1479:265–274
Chiappori F, Pucciarelli S, Merelli I, Ballarini P, Miceli C, Milanesi L (2012) Structural thermal adaptation of β-tubulins from the Antarctic psychrophilic protozoan Euplotes focardii. Proteins 80:1154–1166
Chiuri R, Majorano G, Rizello 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
Cipolla A, Delbrassine F, Da Lage JL, Feller G (2011) Temperature adaptations in psychrophilic, mesophilic and thermophilic chloride-dependent alpha-amylases. Biochimie 94:1943–1950
Cipolla A, D’Amico S, Barumandzadeh R, Matagne A, Feller G (2012) Stepwise adaptation to low temperature as revealed by multiple mutants of psychrophilic α-amylase from Antarctic bacterium. J Biol Chem 286:38348–38355
Collins T, Claverie P, D’Amico S, Georlette D, Gratia E, Hoyoux A, Meuwis MA, Poncin J, Sonan G, Feller G, Gerday C (2002) Life in the cold: psychrophilic enzymes. In: Pandalai SG (ed) Recent research developments in proteins, vol 1. Transworld Research Network, Trivandrum, pp 13–26
Collins T, Meuwis M-A, Gerday C, Feller G (2003) Activity, stability and flexibility in glycosidases adapted to extreme thermal environments. J Mol Biol 338:419–428
Collins T, D’Amico S, Marx J-C, Feller G, Gerday C (2007) Cold-adapted enzymes. In: Gerday C, Glansdorff N (eds) Physiology and biochemistry of extremophiles. ASM Press, Washington, DC, pp 165–179
Collins T, Roulling F, Piette F, Marx J-C, Feller G, Gerday C, D’Amico S (2008) Fundamentals of cold-adapted enzymes. In: Margesin R, Schinner F, Marx J-C, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 211–227
Coquelle N, Fioravanti E, Weik M, Vellieux F, Madern D (2007) Activity, stability and structural studies of lactate dehydrogenases adapted to extreme thermal environments. J Mol Biol 374:547–562
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
D’Amico S, Gerday C, Feller G (2002) Dual effects of an extra disulphide bond on the activity and stability of a cold-adapted α-amylase. J Biol Chem 277:46110–46115
D’Amico S, Marx J-C, Gerday C, Feller G (2003) Activity-stability relationship in extremophilic enzymes. J Biol Chem 278:7891–7896
D’Amico S, Sohier J-S, Feller G (2006a) Kinetics and energetics of ligand binding determined by microcalorimetry: insight into active site mobility in a psychrophilic alpha-amylase. J Mol Biol 358:1296–1304
D’Amico S, Collins T, Marx JC, Feller G, Gerday C (2006b) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389
Daniel RM, Danson MJ (2010) A new understanding of how temperature affects the catalytic activity of enzymes. Trends Biochem Sci 35:584–591
Davail S, Feller G, Narinx E, Gerday C (1994) Cold adaptation of proteins. Purification, characterization, and sequence of the heat labile subtilisin from the Antarctic psychrophile Bacillus TA 41. J Biol Chem 269:17448–17453
De Santi C, Tutino ML, Mandrich L, Giuliani M, Parilli E, Del Vecchio P, De Pascale D (2010) The hormone sensitive lipase from Psychrobacter sp. TA144: new insight in the structure/functional characterization. Biochimie 92:949–957
Demchenko AP, Rusyn OI, Saburova EA (1989) Kinetics of the lactate dehydrogenase reaction in high-viscosity media. Biochim Biophys Acta 998:196–203
Dias CL, Ala-Nissila T, Wong E, Kabut J, Vattulainen I, Grant M, Karttunen M (2010) The hydrophobic effect and its role in cold denaturation. Cryobiology 60:91–99
Eyring H (1935) The activated complex in chemical reactions. J Chem Phys 3:107–115
Fedoy A-E, Yang N, Martinez A, Leiros H-K, Stee H (2007) Structural and functional properties of isocitrate dehydrogenase from the psychrophilic bacterium Desulfotalea psychrophila reveal a cold-active enzyme with an unusual high thermal stability. J Mol Biol 372:130–149
Feller G (2008) Enzyme function at low temperatures in psychrophiles. In: Siddiqui KS, Thomas T (eds) Protein adaptation in extremophiles. Nova Science, New York, NY, pp 35–69
Feller G (2010) Protein stability and enzyme activity at extreme biological temperatures. J Phys Condens 22:32101–32118
Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1:200–208
Feller G, Lonhienne T, Deroanne C, Libioulle C, Van Beeumen J, Gerday C (1992) Purification, characterization, and nucleotide sequence of the thermolabile α-amylase from the Antarctic psychrotroph Alteromonas haloplanktis A 23. J Biol Chem 267:5217–5221
Feller G, Narinx E, Arpigny JL, Zekhnini Z, Swings J, Gerday C (1994) Temperature dependence of growth, enzyme secretion and activity of psychrophilic Antarctic bacteria. Appl Microbiol Biotechnol 41:477–479
Feller G, Zekhnini Z, Lamotte-Brasseur J, Gerday C (1997) Enzymes from cold-adapted microorganisms. The class C beta-lactamase from the Antarctic psychrophile Psychrobacter immobilis A5. Eur J Biochem 244:186–191
Feller G, D’Amico S, Gerday C (1999) Thermodynamic stability of a cold-active α-amylase from the Antarctic bacterium Alteromonas haloplanktis. Biochemistry 38:4613–4619
Fields PA, Somero GN (1998) Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenases A4 orthologs of Antarctic notothenioid fishes. Proc Natl Acad Sci U S A 95:11476–11481
Fields PA, Dong Y, Meng X, Somero GN (2015) Adaptations of protein structure and function to temperature: there is more than one way to ‘skin a cat’. J Exp Biol 2018:1801–1811
Garcia-Viloca M, Gao J, Karplus M, Truhlar DG (2004) How enzymes work: analysis by modern rate theory and computer simulations. Science 303:186–195
Garsoux G, Lamotte-Brasseur J, Gerday C, Feller G (2004) Kinetic and structural optimisation to catalysis at low temperatures in a psychrophilic cellulase from the Antarctic bacterium Pseudoalteromonas haloplanktis. Biochem J 384:247–253
Georlette D, Jonsson ZO, Van Petegem F, Chessa J-P, Van Beeumen J, Hubscher U, Gerday C (2000) A DNA ligase from the psychrophile Pseudoalteromonas haloplanktis gives insights into the adaptation of proteins at low temperatures. Eur J Biochem 267:3502–3512
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
Georlette D, Blaise V, Collins T, D’Amico S, Gratia E, Hoyoux A, Marx J-C, Sonan G, Feller G, Gerday C (2004) Some like it cold: biocatalysis at low temperatures. FEMS Microbiol Rev 28:25–42
Gerday C (2013) Catalysis and protein folding in psychrophiles. In: Yumoto I (ed) Cold-adapted microorganisms. Caister Academic press, Norfolk, pp 137–157
Gerday C (2014) Fundamentals of cold-active enzymes. In: Buzzini P, Margesin R (eds) Cold-adapted yeasts. Springer, Berlin, pp 325–350
Gerike U, Danson MJ, Russell NJ, Hough DW (1997) Sequencing and expression of the gene encoding a cold-active citrate synthase from an Antarctic bacterium strain DS-3R. Eur J Biochem 248:49–57
Gershenson A, Gierasch LM (2011) Protein folding in the cell: challenges and progress. Curr Opin Struct Biol 21:32–41
Goodchild A, Saunders NF, Erlan H, Raftery M, Guilhaus M, Curmi PM, Cavicchioli R (2004) A proteomic determination of cold adaptation in the Antarctic archeon, Methanococcoides burtonii. Mol Microbiol 53:309–321
Gudmundsdóttir A (2002) Cold-adapted and mesophilic brachyurins. Biol Chem 383:1125–1131
Gudmundsdóttir E, Spilliaert R, Yang Q, Craik CS, Bjarnason JB, Gudmundsdóttir A (1996) Isolation and characterization of two cDNAs from Atlantic cod encoding two distinct psychrophilic elastases. Comp Biochem Physiol B 113:795–801
Heidarsson PO, Sigurdsson ST, Asgeirsson B (2009) Structural features and dynamics of a cold-adapted alkaline phosphatase studied by EPR spectroscopy. FEBS J 276:2725–2735
Hess E (1934) Effects of low temperatures on the growth of marine bacteria. Contribs Can Biol Fisheries Ser C 8:491–505
Hochachka PW, Somero GN (1973) Strategies of biochemical adaptation. WB Saunders, Philadelphia, PA
Hochachka PW, Somero GN (2002) Temperature. In: Hochachka PW, Somero GN (eds) Biochemical adaptation. Oxford University Press, New York, NY, 190 pp
Homchaudhuri L, Sarma N, Swaminathan R (2006) Effect of crowding by dextrans and ficols on the rate of alkaline phosphatase-catalysed hydrolysis: a size-dependent investigation. Biopolymers 83:477–486
Huston AL, Krieger-Brockett BB, Deming JW (2000) Remarkably low temperature optima for extracellular enzyme activity from Arctic bacteria sea ice. Environ Microbiol 4:383–388
Huston AL, Haeggström JZ, Feller G (2008) Cold adaptation of enzymes: structural, kinetic and microcalorimetric characterizations of an aminopeptidase from the Arctic psychrophile Colwellia psychrerythraea and of human leukotriene A (4) hydrolase. Biochim Biophys Acta 1784:1865–1872
Ingraham JL, Stokes JL (1959) Psychrophilic bacteria. Bacteriol Rev 23:97–108
Isaksen GV, Aqvist J, Brandsdal BO (2016) Enzyme surface rigidity tunes the temperature dependence of catalytic rates. Proc Natl Acad Sci U S A 113:7822–7827
Kawamoto J, Kurihara T, Kitagawa M, Kato l, Esaki N (2007) Proteomic studies of an Antarctic cold-adapted bacterium, Shewanella livingstonensis AC 10, for global identification of cold-inducible proteins. Extremophiles 10:819-826
Kim HW, Wi AR, Jeon BW, Lee JH, Shin SC, Park H, Jeon SJ (2015) Cold adaptation of a psychrophilic chaperonin from Psychrobacter sp. and its application for heterologous protein expression. Biotechnol Lett 37:1887–1893
Kobori H, Sullivan CW, Shizuya H (1984) Heat-labile alkaline phosphatase from Antarctic bacteria: rapid 5’ end-labeling of nucleic acid. Proc Natl Acad Sci U S A 81:6691–6695
Kobus S, Widderich N, Hoeppner A, Bremer E, Smits SH (2015) Overproduction, crystallization and X-ray diffraction data analysis of ectoine synthase from the cold-adapted marine bacterium Sphingopyxis alaskensis. Acta Cristallogr F Struct Biol Commun 71:1027–1032
Koutsiolis D, Wang E, Tzanodaskalaki M, Nikiforaki D, Deli A, Feller G, Heikinheimo P, Bouriotis V (2008) Directed evolution on the cold adapted properties of TAB5 alkaline phosphatase. Protein Eng 21:319–327
Kuhn E (2012) Toward understanding life under subzero conditions: the significance of exploring psychrophilic “cold-shock” proteins. Astrobiology 12:1078–1086
Kumar S, Tsai CJ, Nussinov R (2002) Maximal stabilities of reversible two-state proteins. Biochemistry 41:5359–5374
Leiros HK, Willassen NP, Smalas AO (2000) Structural comparison of psychrophilic and mesophilic trypsins. Elucidating the molecular basis of cold-adaptation. Eur J Biochem 267:1039–1049
Leopold PE, Montal M, Onuchic JN (1992) Protein folding funnels: a kinetic approach to the sequence-structure relationship. Proc Natl Acad Sci U S A 89:8721–8725
Lonhienne T, Baise E, Feller G, Bouriotis V, Gerday C (2001a) Enzyme activity determination on macromolecular substrates by isothermal calorimetry: application to mesophilic and psychrophilic chitinases. Biochim Biophys Acta 1545:349–356
Lonhienne T, Zoidakis J, Vorgias E, Feller G, Gerday C, Bouriotis V (2001b) Modular structure, local flexibility and cold-activity of a novel chitobiase from a psychrophilic Antarctic bacterium. J Mol Biol 310:291–297
Margesin R (2009) Effect of temperature on growth parameters of psychrophilic bacteria and yeasts. Extremophiles 13:257–262
Marshall CI (1997) Cold-adapted enzymes. Trends Biotechnol 15:359–364
Marx J-C, Collins T, D’Amico S, Feller G, Gerday C (2007) Cold-adapted enzymes from marine Antarctic microorganisms. Mar Biotechnol 9:293–304
Mastro AM, Keith AD (1984) Diffusion in the aqueous compartment. J Cell Biol 99:180–187
Matsuura A, Yao M, Aizawa T, Koganesawa N, Masaki K, Miyazawa M, Demura M, Tanaka I, Kawano K, Nitta K (2002) Structural analysis of an insect lysozyme exhibiting catalytic efficiency at low temperature. Biochemistry 41:12086–12092
Mereghetti P, Riccardi L, Brandsdal BO, Fantucci P, De Gioia L, Papaleo E (2010) Near native-state conformational landscape of psychrophilic and mesophilic enzymes: probing the folding funnel model. J Phys Chem B 114:7609–7619
Miao LL, Hou YJ, Fan HX, Qu J, Qi C, Liu Y, Li DF, Liu ZP (2016) Molecular structural basis for the cold adaptedness of the psychrophilic β-Glucosidase BgIU in Micrococcus antarcticus. Appl Environ Microbiol 82:2021–2030
Miyazaki K, Wintrode PL, Grayling RA, Rubigh DN, Arnold FH (2000) Directed evolution study of temperature adaptation in a psychrophilic enzyme. J Mol Biol 297:1015–1026
Moe E, Leiros I, Rijse EK, Olufsen M, Lanes O, Smalas A, Willassen NP (2004) Optimisation of the surface electrostatics as a strategy for cold adaptation of uracil-DNA N-glycosylase. J Mol Biol 343:1221–1230
Mykytczuk NC, Trevors JT, Foote SJ, Leduc LG, Ferroni GD, Twine SM (2011) Proteomic insight into cold adaptation of psychrotrophic and mesophilic Acidithiobacillus ferrooxidans strains. Antonie Van Leeuwenhoek 100:259–277
Naicker MC, Seul JI, Im H (2012) Identification of chaperones in freeze tolerance in Saccharomyces cerevisiae. J Microbiol 50:882–887
Narinx E, Baise E, Gerday C (1997) Subtilisin from Antarctic bacteria: characterization and site-directed mutagenesis of residues possibly involved in the adaptation to cold. Protein Eng 10:1271–1279
Pace CN, Laurents DV (1989) A new method for determining the heat capacity change for protein folding. Biochemistry 28:2520–2525
Papaleo E, Olufsen M, De Gioia L, Bransdal BO (2007) Optimization of electrostatics as a strategy for cold-adaptation: a case study of cold- and warm-active elastases. J Mol Graph Model 26:93–103
Papaleo E, Pasi M, Tiberti M, De Gioia L (2011) Molecular dynamics of mesophilic-like mutants of a cold-adapted enzyme: insight into distal effects induced by the mutations. PLoS ONE 6:e24214
Paredes DI, Watters K, Pitman DJ, Bystrff C, Dordick JS (2011) Comparative void-volume analysis of psychrophilic and mesophilic enzymes: structural bioinformatics of psychrophilic enzymes reveals sources of core flexibility. BMC Struct Biol 11:42
Petrescu I, Lamotte-Brasseur J, Chessa J-P, Ntarima P, Claeyssens M, Devreese B, Marino G, Gerday C (2000) Xylanase from the psychrophilic yeast Cryptococcus adeliae. Extremophiles 4:137–144
Piette F, D’Amico S, Struvay C, Mazzuchelli G, Remaut J, Tutino ML, Danchin A, Leprince P, Feller G (2010) Proteomics of life at low temperature: trigger factor is the primary chaperone in the Antarctic bacterium Pseudoalteromonas haloplanktis TAC 125. Mol Microbiol 76:120–132
Piette F, Struvay C, Feller G (2011) The protein folding in psychrophiles: facts and current issues. Environ Microbiol 13:1924–1933
Qiu Y, Kathariou S, Lubman DM (2006) Proteomic analysis of cold adaptation in a Siberian permafrost bacterium Exiguobacterium sibiricum 255-15 by two-dimensional liquid separation coupled with mass spectrometry. Proteomics 6:135–148
Qoura F, Elleuche S, Brueck T, Antranikian G (2014) Purification and characterization of a cold-adapted pullulanase from a psychrophilic bacterial isolate. Extremophiles 18:1095–1102
Radestock S, Gohlke H (2011) Protein rigidity and thermophilic adaptation. Proteins 79:1089–1108
Ramli AN, Mahadi NM, Shamsir MS, Rabu A, Joyce-Tan KH, Murad AM, Illias RM (2012) Structural prediction of a novel chitinase from the psychrophilic Glaciozyma antarctica PI12 and an analysis of its structural properties and function. J Comput Aided Mol Des 26:947–961
Rodrigues DF, Ivanova N, He Z, Huebner M, Zhou J, Tiedje JM (2008) Architecture of thermal adaptation in Exiguobacterium sibiricum strain isolated from 3 million years old permafrost: a genome and transcriptome approach. BMC Genom 9:547
Roman EA, Faraj SE, Cousido-Siah A, Mitscler A, Podjarny A, Santos J (2013) Frataxin from Psychromonas ingrahamii as a model to study stability modulation within the CYaY protein family. Biochim Biophys Acta 1834:1168–1180
Russell NJ (2000) Toward a molecular understanding of cold activity of enzymes from psychrophiles. Extremophiles 4:83–90
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
Santarossa G, Gatti-Lafranconi P, Alquati C, De Gioia L, Alberghina L, Fantucci P, Lotti M (2005) Mutations in the « lid » region affect chain length specificity and thermostability of a Pseudomonas fragi lipase. FEBS Lett 579:2383–2386
Santiago M, Ramírez-Sarmiento CA, Zamora RA, Parra LP (2016) Discovery, molecular mechanisms, and industrial applications of cold-active enzymes. Front Microbiol 7:1408
Sato Y, Watanabe S, Yamaoka N, Takada Y (2008) Gene cloning of cold-adapted isocitrate lyase from a psychrophilic bacterium, Colwellia psychrerythraea, and analysis of amino acid residues involved in cold adaptation of this enzyme. Extremophiles 12:107–117
Schmidt-Nielsen S (1902) Ueber einige psychrophile Mikrooganismen und ihr Vorkommen. Centr Bakteriol Parasitenk Abt II 9:145–147
Schwartz MH, Pan T (2016) Temperature dependent mistranslation in a hyperthermophile adapts proteins to lower temperature. Nucleic Acids Res 44:294–303
Serrano L, Fersht AR (1989) Capping and alpha-helix stability. Nature 342:296–299
Siddiqui KS, Cavicchioli R (2006) Cold-adapted enzymes. Annu Rev Biochem 75:403–433
Siddiqui KS, Bokhari SA, Afzal AJ, Singh S (2004) A novel thermodynamic relationship based on Kramers Theory for studying enzyme kinetics under high viscosity. IUBMB Life 56:403–407
Sigtryggsdóttir AR, Papaleo E, Thorbjarnardóttir SH, Kristjánsson MM (2014) Flexibility of cold-and-heat adapted subtilisin-like serine proteinase evaluated with fluorescence quenching and molecular dynamics. Biochim Biophys Acta 1844:705–712
Simpson PJL, Codd R (2011) Cold adaptation of the mononuclear molybdoenzyme periplasmic nitrate reductase from the Antarctic bacterium Shewanella gelidimarina. Biochem Biophys Res Commun 414:783–788
Smalas AO, Leiros HK, Os V, Willassen NP (2000) Cold-adapted enzymes. Biotechnol Annu Rev 6:1–57
Somero GN (1977) Temperature as a selective factor in protein evolution: the adaptational strategy of compromise. J Exp Zool 194:175–188
Somero GN (1995) Proteins and temperature. Annu Rev Physiol 57:43–68
Sonan GK, Receveur-Brechot V, Duez C, Aghajari N, Czjzek M, Haser R, Gerday C (2007) The linker region plays a key role in the adaptation to cold of the cellulase from an Antarctic bacterium. Biochem J 407:293–302
Sotelo-Mundo RR, Lopez-Zavala AA, Garcia-Orozco KD, Arvizu AA, Velazquez-Contreras EF, Valenzuela-Soto EM, Rojo-Dominguez A, Kanost MR (2007) The lysozyme from insect (Manduca sexta) is a cold-adapted enzyme. Protein Pept Lett 14:774–778
Spiwok V, Lipovova P, Skalova T, Duskova J, Dohnalek J, Hasek J, Russell N, Kralova B (2007) Cold-active enzymes studied by comparative molecular dynamics simulation. J Mol Model 13:485–497
Stadler AM, Garvey CJ, Bocahut A, Sacquin-Mora S, Digel I, Schneider GJ, Natali F, Artmann GM, Zaccai G (2012) Thermal fluctuations of haemoglobin from different species: adaptation to temperature via conformational dynamics. J R Soc Interface 7:2845–2855
Sun-Yong K, Kwang-Yeon H, Sung-Hou K, Ha-Chin S, Ye-Sun H, Yunge C (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
Suzuki Y, Haruki M, Takano K, Morikawa M, Kanaya S (2004) Possible involvement of an FKBP family member protein from a psychrotrophic bacterium, Shewanella sp. SLB1 in cold adaptation. J Biochem 271:1372–1381
Suzuki T, Yamamoto K, Tada H, Uda K (2012) Cold-adapted features of arginine kinase from the deep-sea Calyptogena kaikoi. Mar Biotechnol 14:294–303
Talla-Singh D, Stites WE (2008) Refinement of noncalorimetric determination of the change in heat capacity, ΔCp, of protein unfolding and validation across a wide temperature range. Proteins 71:1607–1616
Tang MA, Motoshima H, Watanabe K (2014) Cold adaptation: structural and functional characterizations of psychrophilic and mesophilic acetate kinase. Protein J 33:313–322
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
Thomas T, Cavicchioli R (1998) Archaeal cold-adapted proteins: structural and evolutionary analysis of elongation factor 2 proteins from psychrophilic, mesophilic and thermophilic methanogens. FEBS Lett 439:281–286
Tiberti M, Papaleo E (2011) Dynamic properties of extremophilic subtilisin-like serine-proteases. J Struct Biol 174:69–83
Tindbaek N, Svendsen A, Oestezrgaard PR, Draborg H (2004) Engineering a substrate-specific cold-adapted subtilisin. Protein Eng Des Sel 17:149–156
Ting L, Williams TJ, Cowley MJ, Lauro FM, Guilhaus M, Raftery MJ, Cavicchioli R (2010) Cold adaptation in the marine bacterium, Sphingopyxis alaskensis assessed using quantitative proteomics. Environ Microbiol 12:2658–2676
Truongvan N, Jang SH, Lee CW (2016) Flexibility and stability trade-off in active site of cold-adapted Pseudomonas mandelii esterase EstK. Biochemistry 55:3542–3549
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
Vester JK, Glaring MA, Stougaard P (2015) An exceptionally cold-adapted alpha-amylase from a metagenomics library of a cold and alkaline environment. Appl Microbiol Biotechnol 99:717–727
Vieille C, Zeikus G (2001) Hyperthermophilic enzymes: sources, uses and molecular mechanisms for thermostability. Microbiol Mol Biol Rev 65:1–43
Watanabe S, Yasutake Y, Tanaka I, Takada Y (2005) Elucidation of stability determinants of cold-adapted monomeric isocitrate dehydrogenase from a psychrophilic bacterium, Colwellia maris, by construction of chimeric enzymes. Microbiology 151:1083–1094
Wintrode PL, Miyazaki K, Arnold FH (2001) Patterns of adaptation in a laboratory evolved thermophilic enzyme. Biochim Biophys Acta 1549:1–8
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 metalloprotease 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
Xu Y, Feller G, Gerday C, Glansdorff N (2003a) Moritella cold-active dihydrofolate reductase: are there natural limits to optimization of catalytic efficiency at low temperature. J Bacteriol 185:5519–5526
Xu Y, Feller G, Gerday C, Glansdorff N (2003b) Metabolic enzymes from psychrophilic bacteria: challenge of adaptation to low temperatures in ornithine carbamoyltransferase from Moritella abyssi. J Bacteriol 185:2161–2168
Yang J, Li J, Mai Z, Tian X, Zhang S (2013) Purification, characterization, and gene cloning of a cold-adapted thermolysin-like protease from Halobacillus sp. SCSIO 20089. J Biosci Bioeng 115:628–632
Yusof NA, Hashim NH, Beddoe T, Mahadi NM, Ililias RM, Bakar FD, Murad AM (2016) Thermotolerance and molecular chaperone function of an SGT1-like protein from the psychrophilic yeast, Glaciozyma Antarctica. Cell Stress Chaperones 4:707–715
Zheng S, Ponder MA, Shih JY, Tiedje JM, Thomashow MF, Lubman DM (2007) A proteomic analysis of Psychrobacter arcticus 273-4 adaptation to low temperature and salinity using 2-D liquid mapping approach. Electrophoresis 28:467–488
Zheng Y, Li Y, Liu W, Chen CC, Ko TP, He M, Xu Z, Liu M, Luo H, Guo RT, Yao B, Ma Y (2016) Structural insight into potential cold adaptation mechanism through a psychrophilic glycoside hydrolase family 10 endo-β-1,4-xylanase. J Struct Biol 193:206–211
Zhong CQ, Song S, Fang N, Liang X, Zhu H, Tang XF, Tang B (2009) Improvement of low-temperature caseinolytic activity of a thermophilic subtilase by directed evolution and site directed mutagenesis. Biotechnol Bioeng 104:862–870
Acknowledgements
Tony Collins is supported by the FCT, the European Social Fund, the Programa Operacional Potencial Humano and the Investigador FCT Programme (IF/01635/2014). The FCT is thanked for their funding through EXPL/BBB-BIO/1772/2013-FCOMP-01-0124-FEDER-041595, the strategic programme UID/BIA/04050/2013 (POCI-01-0145-FEDER-007569), and the ERDF through COMPETE2020—Programa Operacional Competitividade e Internacionalização (POCI). All the technical staff at the CBMA is thanked for the skillful technical assistance.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Collins, T., Gerday, C. (2017). Enzyme Catalysis in Psychrophiles. In: Margesin, R. (eds) Psychrophiles: From Biodiversity to Biotechnology. Springer, Cham. https://doi.org/10.1007/978-3-319-57057-0_10
Download citation
DOI: https://doi.org/10.1007/978-3-319-57057-0_10
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-57056-3
Online ISBN: 978-3-319-57057-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)