Function and biotechnology of extremophilic enzymes in low water activity

Aquatic Biosystems

Ram Karan¹  Melinda D Capes¹  Shiladitya DasSarma¹ 

[1] Institute of Marine and Environmental Technology, University System of Maryland, Baltimore, MD, USA

关键词: Bioenergy;    Biofuel;    High salinity;    Low temperature;    Organic solvent;    Cold activity;    Psychrophile;    Halophiles;    Protein stability;    Extremozymes;    Extremophile;   

Others  :  794760
DOI  :  10.1186/2046-9063-8-4

 received in 2011-11-14, accepted in 2012-02-02,  发布年份 2012

【 摘 要 】

Enzymes from extremophilic microorganisms usually catalyze chemical reactions in non-standard conditions. Such conditions promote aggregation, precipitation, and denaturation, reducing the activity of most non-extremophilic enzymes, frequently due to the absence of sufficient hydration. Some extremophilic enzymes maintain a tight hydration shell and remain active in solution even when liquid water is limiting, e.g. in the presence of high ionic concentrations, or at cold temperature when water is close to the freezing point. Extremophilic enzymes are able to compete for hydration via alterations especially to their surface through greater surface charges and increased molecular motion. These properties have enabled some extremophilic enzymes to function in the presence of non-aqueous organic solvents, with potential for design of useful catalysts. In this review, we summarize the current state of knowledge of extremophilic enzymes functioning in high salinity and cold temperatures, focusing on their strategy for function at low water activity. We discuss how the understanding of extremophilic enzyme function is leading to the design of a new generation of enzyme catalysts and their applications to biotechnology.

【 授权许可】

   
2012 Karan et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Hough DW, Danson MJ: Extremozymes. Curr Opin Chem Biol 1999, 1:39-46.
• [2]Gomes J, Steiner W: The biocatalytic potential of extremophiles and extremozymes. Food Technol Biotechnol 2004, 42:223-235.
• [3]Vieille C, Zeikus GJ: Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol Mol Biol Rev 2001, 1:1-43.
• [4]Bull AT, Ward AC, Goodfellow M: Search and discovery strategies for biotechnology: the paradigm shift. Microbiol Mol Biol Rev 2000, 3:573-606.
• [5]Iyer PV, Ananthanarasyan L: Enzyme stability and stabilization-aqueous and non-aqueous environment. Process Biochem 2008, 43:1019-1032.
• [6]Kaul P, Asano Y: Strategies for discovery and improvement of enzyme function: state of the art and opportunities. Microb Biotechnol 2011. doi: 10.1111/j.1751-7915.2011.00280.x
• [7]Adams MWW, Perler FB, Kelly RM: Extremozymes: Expanding the limits of biocatalysis. Nat Biotechnol 1995, 13:662-668.
• [8]DasSarma P, Coker JA, Huse V, DasSarma S: Halophiles, Biotechnology. In Encyclopedia of Industrial Biotechnology, Bioprocess, Bioseparation, and Cell Technology. Edited by Flickinger MC. Hoboken, NJ: John Wiley and Sons; 2010:2769-2777.
• [9]Bowers KJ, Mesbah NM, Wiegel J: Biodiversity of poly-extremophilic bacteria: Does combining the extremes of high salt, alkaline pH and elevated temperature approach a physico-chemical boundary for life? Saline Syst 2009, 5:9-17.
• [10]Marhuenda-Egea FC, Bonete MJ: Extreme halophilic enzymes in organic solvents. Curr Opin Biotechnol 2002, 13:385-389.
• [11]Pire C, Marhuenda-egea FC, Esclapez J, Alcaraz L, Ferrer J, Bonete MJ: Stability and enzymatic studies of glucose dehydrogenase from the Archaeon Haloferax mediterranei in reverse micelles. Biocatal Biotransform 2004, 22:17-23.
• [12]Danson MJ, Hough DW: The structural basis of protein halophilicity. Comp Biochem Physiol A Physiol 1997, 117:307-312.
• [13]Kennedy SP, Ng WV, Salzberg SL, Hood L, DasSarma S: Understanding the adaptation of Halobacterium species NRC-1 to its extreme environment through computational analysis of its genome sequence. Genome Res 2001, 11:1641-1650.
• [14]Siddiqui KS, Cavicchioli R: Cold-adapted enzymes. Annu Rev Biochem 2006, 75:403-433.
• [15]Kuntz ID: Hydration of macromolecules IV Polypeptide conformation in frozen solutions. J Am Chem Soc 1971, 93:516-518.
• [16]Saenger W: Structure and dynamics of water surrounding biomolecules. Annu Rev Biophys Biophys Chem 1987, 16:93-114.
• [17]Persson E, Halle B: Cell water dynamics on multiple time scales. Proc Natl Acad Sci USA 2008, 17:6266-6271.
• [18]Spitzer J: From water and ions to crowded biomacromolecules: In vivo structuring of a prokaryotic cell. Microbiol Mol Biol R 2011, 3:491-506.
• [19]Zaccai G: The effect of water on protein dynamics. Philos Trans R Soc Lond B Biol Sci 2004, 359:1269-1275.
• [20]Mountain RD, Thirumalai D: Alterations in water structure induced by guanidinium and sodium ions. J Phys Chem 2004, 108:19711-19716.
• [21]Mancinelli R, Botti A, Bruni F, Ricci MA, Soper AK: Hydration of sodium, potassium, and chloride ions in solution and the concept of structure maker/breaker. Phys Chem 2007, 111:13570-13577.
• [22]Bakker HJ: Water dynamics: Ion-ing out the details. Nature Chemistry 2009, 1:24-25.
• [23]Irimia A, Ebel C, Madern D, Richard SB, Cosenza LW, Zaccaï G, Vellieux FM: The oligomeric states of Haloarcula marismortui malate dehydrogenase are modulated by solvent components as shown by crystallographic and biochemical studies. J Mol Biol 2003, 3:859-873.
• [24]Dennis PP, Shimmin LC: Evolutionary divergence and salinity-mediated selection in halophilic archaea. Microbiol Mol Biol Rev 1997, 61:90-104.
• [25]Sedlák E, Stagg L, Wittung-Stafshede P: Role of cations in stability of acidic protein Desulfovibrio desulfuricans apoflavodoxin. Arch Biochem Biophys 2008, 1:128-135.
• [26]Ortega G, Laín A, Tadeo X, López-Méndez B, Castaño D, Millet O: Halophilic enzyme activation induced by salts. Scientific Reports 2011, 1:6.
• [27]Paul S, Bag SK, Das S, Harvill ET, Dutta C: Molecular signature of hypersaline adaptation: Insights from genome and proteome composition of halophilic prokaryotes. Genome Biol 2008, 9:R70.
• [28]Dym O, Mevarech M, Sussman JL: Structural features that stabilize halophilic malate dehydrogenase from an archaebacterium. Science 1995, 267:1344-1346.
• [29]Frolow F, Harel M, Sussman JL, Mevarech M, Shoham M: Insights into protein adaptation to a saturated salt environment from the crystal structure of a halophilic 2Fe-2S ferredoxin. Nature Struct Biol 1996, 3:452-458.
• [30]Britton KL, Baker PJ, Fisher M, Ruzheinikov S, Gilmour DJ, Bonete MJ, Ferrer J, Pire C, Esclapez J, Rice DW: Analysis of protein solvent interactions in glucose dehydrogenase from the extreme halophile Haloferax mediterranei. Proc Natl Acad Sci USA 2006, 103:4846-4851.
• [31]Lanyi JK: Salt dependent properties of proteins from extremely halophilic bacteria. Bacteriol Rev 1974, 38:272-290.
• [32]Madern D, Ebel C, Zaccai G: Halophilic adaptation of enzymes. Extremophiles 2000, 4:91-98.
• [33]Fukuchi S, Yoshimune K, Wakayama M, Moriguchi M, Nishikawa K: Unique amino acid composition of proteins in halophilic bacteria. J Mol Biol 2003, 327:347-357.
• [34]Bolhuis A, Kwan D, Thomas JR: Halophilic adaptations of proteins. In Protein adaptation in extremophiles. Edited by Siddiqui KS, Thomas T. New York: Nova Science Publishers Inc USA; 2008:71-104.
• [35]Tadeo X, López-Méndez B, Trigueros T, Laín A, Castaño D, Millet O: Structural basis for the amino acid composition of proteins from halophilic archaea. PLoS Biol 2009, 7:e1000257.
• [36]Ishibashi M, Tokunaga H, Hiratsuka K, Yonezawa Y, Tsurumaru H, Arakawa T, Tokunaga M: NaCl-activated nucleoside diphosphate kinase from extremely halophilic archaeon, Halobacterium salinarum, maintains native conformation without salt. FEBS Lett 2001, 493:134-138.
• [37]De Castro RE, Ruiz DM, Giménez MI, Silveyra MX, Paggi RA, Maupin-Furlow JA: Gene cloning and heterologous synthesis of a haloalkaliphilic extracellular protease of Natrialba magadii (Nep). Extremophiles 2008, 5:677-687.
• [38]Kastritis PL, Papandreou NC, Hamodrakas SJ: Haloadaptation: insights from comparative modeling studies of halophilic archaeal DHFRs. Int J Biol Macromol 2007, 41:447-453.
• [39]Elcock AH, McCammon JA: Electrostatic contributions to the stability of halophilic proteins. J Mol Biol 1998, 4:731-748.
• [40]Mevarech M, Frolow F, Gloss LM: Halophilic enzymes: Proteins with a grain of salt. Biophys Chem 2000, 86:155-164.
• [41]Pieper U, Kapadia G, Mevarech M, Herzberg O: Structural features of halophilicity derived from the crystal structure of dihydrofolate reductase from the Dead Sea halophilic archaeon, Haloferax volcanii. Structure 1998, 6:75-88.
• [42]Winter JA, Christofi P, Morroll S, Bunting KA: The crystal structure of Haloferax volcanii proliferating cell nuclear antigen reveals unique surface charge characteristics due to halophilic adaptation. BMC Struct Biol 2009, 9:55.
• [43]Müller-Santos M, de Souza EM, Pedrosa Fde O, Mitchell DA, Longhi S, Carrière F, Canaan S, Krieger N: First evidence for the salt-dependent folding and activity of an esterase from the halophilic archaea Haloarcula marismortui. Biochim Biophys Acta 2009, 1791:719-729.
• [44]Esclapez J, Pire C, Bautista V, Martínez-Espinosa RM, Ferrer J, Bonete MJ: Analysis of acidic surface of Haloferax mediterranei glucose dehydrogenase by site-directed mutagenesis. FEBS Lett 2007, 581:837-842.
• [45]Rao JKM, Argos P: Structural stability of halophilic proteins. Biochemistry 1981, 20:6536-6543.
• [46]Zaccai G, Cendrin F, Haik Y, Borochov N, Eisenberg H: Stabilization of halophilic malate dehydrogenase. J Mol Biol 1989, 208:491-500.
• [47]Madern D, Camacho M, Rodríguez-Arnedo A, Bonete MJ, Zaccai G: Salt-dependent studies of NADP-dependent isocitrate dehydrogenase from the halophilic archaeon Haloferax volcanii. Extremophiles 2004, 5:377-384.
• [48]Bandyopadhyay AK, Sonawat HM: Salt dependent stability and unfolding of [Fe2-S2] ferredoxin of Halobacterium salinarum: Spectroscopic investigations. Biophys J 2000, 79:501-510.
• [49]Rao L, Zhao X, Pan F, Li Y, Xue Y, Ma Y, Lu JR: Solution behavior and activity of a halophilic esterase under high salt concentration. PLoS One 2009, 9:e6980.
• [50]Jolley KA, Russell RJ, Hough DW, Danson MJ: Site-directed mutagenesis and halophilicity of dihydrolipoamide dehydrogenase from the halophilic archaeon, Haloferax volcanii. Eur J Biochem 1997, 2:362-368.
• [51]Okamoto DN, Kondo MY, Santos JA, Nakajima S, Hiraga K, Oda K, Juliano MA, Juliano L, Gouvea IE: Kinetic analysis of salting activation of a subtilisin-like halophilic protease. Biochim Biophys Acta 2009, 1794:367-373.
• [52]Yamamura A, Ichimura T, Kamekura M, Mizuki T, Usami R, Makino T, Ohtsuka J, Miyazono K, Okai M, Nagata K, Tanokura M: Molecular mechanism of distinct salt-dependent enzyme activity of two halophilic nucleoside diphosphate kinases. Biophys J 2009, 96:4692-4700.
• [53]Srimathi S, Jayaraman G, Feller G, Danielsson B, Narayanan PR: Intrinsic halotolerance of the psychrophilic alpha-amylase from Pseudoalteromonas haloplanktis. Extremophiles 2007, 11:505-515.
• [54]O'Brien R, DeDecker B, Fleming K, Sigler PB, Ladbury JE: The effects of salt on the TATA binding protein-DNA interaction from a hyperthermophilic archaeon. J Mol Biol 1998, 279:117-125.
• [55]Bergqvist S, O'Brien R, Ladbury JE: Site-specific cation binding mediates TATA binding protein-DNA interaction from a hyperthermophilic archaeon. Biochemistry 2001, 40:2419-2425.
• [56]Bergqvist S, Williams MA, O'Brien R, Ladbury JE: Reversal of halophilicity in a protein-DNA interaction by limited mutation strategy. Structure 2002, 10:629-637.
• [57]Bergqvist S, Williams MA, O'Brien R, Ladbury JE: Halophilic adaptation of protein-DNA interactions. Biochem Soc Trans 2003, 31:677-680.
• [58]Sivakumar N, Li N, Tang JW, Patel BK, Swaminathan K: Crystal structure of AmyA lacks acidic surface and provide insights into protein stability at poly-extreme condition. FEBS Lett 2006, 11:2646-2652.
• [59]Altermark B, Helland R, Moe E, Willassen NP, Smalås AO: Structural adaptation of endonuclease I from the cold-adapted and halophilic bacterium Vibrio salmonicida. Acta Crystallogr D Biol Crystallogr 2008, 64:368-376.
• [60]Zhong D, Pal SK, Zewail AH: Biological water: A critique. Chem Phys Lett 2010, 503:1-11.
• [61]Fernández A, Scheraga HA: Insufficiently dehydrated hydrogen bonds as determinants of protein interactions. Proc Natl Acad Sci USA 2003, 100:113-118.
• [62]Kurkal-Siebert V, Daniel RM, L Finney J, Tehei M, Dunn RV, Smith JC: Enzyme hydration, activity and flexibility: A neutron scattering approach. J Non-Cryst Solids 2006, 352:4387-4393.
• [63]Chaplin M: Do we underestimate the importance of water in cell biology? Nat Rev Mol Cell Biol 2006, 11:861-866.
• [64]Koizumi M, Hirai H, Onai T, Inoue K, Hirai M: Collapse of the hydration shell of a protein prior to thermal unfolding. J Appl Cryst 2007, 40:s175-s178.
• [65]Lopez CF, Darst RK, Rossky PJ: Mechanistic elements of protein cold denaturation. J Phys Chem B 2008, 112:5961-5967.
• [66]Dias CL, Ala-Nissila T, Wong-ekkabut J, Vattulainen I, Grant M, Karttunen M: The hydrophobic effect and its role in cold denaturation. Cryobiol 2010, 60:91-99.
• [67]Fields PA: Protein function at thermal extremes: balancing stability and flexibility. Comp Biochem Physiol Pt A 2001, 129:417-431.
• [68]D'Amico S, Collins T, Marx JC, Feller G, Gerday C: Psychrophilic microorganisms: challenges for life. EMBO Rep 2006, 7:385-389.
• [69]Demchenko AP, Ruskyn OI, Saburova EA: Kinetics of the lactate dehydrogenase reaction in high-viscosity media. Biochim Biophys Acta 1989, 998:196-203.
• [70]Siddiqui KS, Bokhari SA, Afzal AJ, Singh S: A novel thermodynamic relationship based on Kramers theory for studying enzyme kinetics under high viscosity. IUBMB Life 2004, 56:403-407.
• [71]Marx JC, Collins T, D'Amico S, Feller G, Gerday C: Cold-adapted enzymes from marine Antarctic microorganisms. Mar Biotechnol (NY) 2007, 9:293-304.
• [72]Georlette D, Blaise V, Collins T, D'Amico S, Gratia E, Hoyoux A, Marx JC, Sonan G, Feller G, Gerday C: Some like it cold: biocatalysis at low temperatures. FEMS Microbiol Rev 2004, 28:25-42.
• [73]Rasmussen BF, Stock AM, Ringe D, Petsko GA: Crystalline ribonuclease: A loses function below the dynamical transition at 220 K. Nature 1992, 357:423-424.
• [74]Siglioccolo A, Gerace R, Pascarella S: "Cold spots" in protein cold adaptation: Insights from normalized atomic displacement parameters (B'-factors). Biophys Chem 2010, 153:104-114.
• [75]Merlino A, Russo Krauss I, Castellano I, De Vendittis E, Rossi B, Conte M, Vergara A, Sica F: Structure and flexibility in cold-adapted iron superoxide dismutases: the case of the enzyme isolated from Pseudoalteromonas haloplanktis. J Struct Biol 2010, 172:343-352.
• [76]Margesin R, Feller G: Biotechnological applications of psychrophiles. Environ Technol 2010, 31:835-844.
• [77]Mavromatis K, Feller G, Kokkinidis M, Bouriotis V: Cold adaptation of a psychrophilic chitinase: a mutagenesis study. Protein Eng 2003, 16:497-503.
• [78]Aurilia V, Rioux-Dubé JF, Marabotti A, Pézolet M, D'Auria S: Structure and dynamics of cold-adapted enzymes as investigated by FT-IR spectroscopy and MD. The case of an esterase from Pseudoalteromonas haloplanktis. J Phys Chem B 2009, 113:7753-7761.
• [79]D'Amico S, Gerday C, Feller G: Activity stability relationships in extremophilic enzymes. J Biol Chem 2003, 278:7891-7896.
• [80]Somero GN: Temperature as a selective factor in protein evolution: The adaptational strategy of "compro-mise". J exp Zool 1975, 194:175-188.
• [81]Feller G, Narinx E, Arpigigny JL, Aittaleb M, Baise E, Genicot S, Gerday C: Enzymes from psychrophilic organisms. FEMS Microbiol Rev 1996, 18:189-202.
• [82]Feller G, Gerday C: Psychrophilic enzymes: molecular basis of cold adaptation. Cell Mol Life Sci 1997, 53:830-841.
• [83]Fields PA, Somero GN: Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A4 orthologs of Antarctic notothenioid fishes. Proc Natl Acad Sci USA 1998, 95:11476-11481.
• [84]Koutsioulis D, Wang E, Tzanodaskalaki M, Nikiforaki D, Deli A, Feller G, Heikinheimo P, Bouriotis V: Directed evolution on the cold adapted properties of TAB5 alkaline phosphatase. Protein Eng Des Sel 2008, 21:319-327.
• [85]Bae E, Phillips GN Jr: Structures and analysis of highly homologous psychrophilic, mesophilic, and thermophilic adenylate kinases. J Biol Chem 2004, 27:28202-28208.
• [86]Aghajari N, Feller G, Gerday C, Haser R: Structures of the psychrophilic Alteromonas haloplanctis α-amylase give insights into cold adaptation at a molecular level. Structure 1998, 6:1503-1516.
• [87]Michaux C, Massant J, Kerff F, Frère JM, Docquier JD, Vandenberghe I, Samyn B, Pierrard A, Feller G, Charlier P, Van Beeumen J, Wouters J: Crystal structure of a cold-adapted class C beta-lactamase. FEBS J 2008, 8:1687-1697.
• [88]Kim SY, Hwang KY, Kim SH, Sung HC, Han YS, 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.
• [89]Sælensminde G, Halskau Ø Jr, Jonassen I: Amino acid contacts in proteins adapted to different temperatures: hydrophobic interactions and surface charges play a key role. Extremophiles 2009, 1:11-20.
• [90]Russell NJ: Toward a molecular understanding of cold activity of enzymes from psychrophiles. Extremophiles 2000, 4:83-90.
• [91]Zartler ER, Jenney FE Jr, Terrell M, Eidsness MK, Adams MW, Prestegard JH: Structural basis for thermostability in aporubredoxins from Pyrococcus furiosus and Clostridium pasteurianum. Biochemistry 2001, 40:7279-7290.
• [92]Feller G: Molecular adaptations to cold in psychrophilic enzymes. Cell Mol Life Sci 2003, 60:648-662.
• [93]Pedersen HL, Willassen NP, Leiros I: The first structure of a cold-adapted superoxide dismutase (SOD): biochemical and structural characterization of iron SOD from Aliivibrio salmonicida. Acta Crystallogr Sect F Struct Biol Cryst Commun 2009, 2:84-92.
• [94]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, 26:17448-17453.
• [95]Feller G, Zekhnini Z, Lamotte-Brasseur J, Gerday C: Enzymes from cold-adapted microorganisms. The class C beta-lactamase from the antarctic psychrophile Psychrobacter immobilis A5. Eur J Biochem 1997, 1:186-191.
• [96]Russell RJ, Gerike U, Danson MJ, Hough DW, Taylor GL: Structural adaptations of the cold-active citrate synthase from an Antarctic bacterium. Structure 1998, 3:351-361.
• [97]Feller G, D'Amico D, Gerday C: Thermodynamic stability of a cold-active alpha-amylase from the Antarctic bacterium Alteromonas haloplanctis. Biochemistry 1999, 14:4613-4619.
• [98]Alvarez M, Zeelen JP, Mainfroid V, Rentier-Delrue F, Martial JA, Wyns L, Wierenga RK, Maes D: Triose-phosphate isomerase (TIM) of the psychrophilic bacterium Vibrio marinus kinetic and structural properties. J Biol Chem 1998, 273:2199-206.
• [99]Cavicchioli R, Charlton T, Ertan H, Omar SM, Siddiqui KS, Williams TJ: Biotechnological uses of enzymes from psychrophiles. Microb Biotechnol 2011, 4:449-460.
• [100]Fjerbaek L, Christensen KV, Norddahl B: A review of the current state of biodiesel production using enzymatic transesterification. Biotechnol Bioeng 2009, 5:1298-1315.
• [101]Lee K-T, Foglia TA, Chang KS: Production of alkyl ester as biodiesel from fractionated lard and restaurant grease. J AmOil Chem Soc 2002, 2:191-195.
• [102]Lee DH, Kim JM, Shin HY, Kang SW, Kim SW: Biodiesel production using a mixture of immobilized Rhizopus oryzae and Candida rugosa lipases. Biotechnol Bioprocess Eng 2006, 6:522-525.
• [103]Lee JH, Kim SB, Kang SW, Song YS, Park C, Han SO, Kim SW: Biodiesel production by a mixture of Candida rugosa and Rhizopus oryzae lipases using a supercritical carbon dioxide process. Bioresour Technol 2011, 2:2105-2108.
• [104]Deng L, Xu XB, Haraldsson GG, Tan TW, Wang F: Enzymatic production of alkyl esters through alcoholysis: A critical evaluation of lipases and alcohols. J Am Oil Chem Soc 2005, 5:341-347.
• [105]Tan TW, Nie KL, Wang F: Production of biodiesel by immobilized Candida sp. lipase at high water content. Appl Biochem Biotechnol 2006, 2:109-116.
• [106]Kumari V, Shah S, Gupta MN: Preparation of biodiesel by lipasecatalyzed transesterification of high free fatty acid containing oil from Madhuca indica. Energy Fuels 2007, 1:368-372.
• [107]Shah S, Gupta MN: Lipase catalyzed preparation of biodiesel from Jatropha oil in a solvent-free system. Process Biochem 2007, 3:409-414.
• [108]Gupta A, Khare SK: Enzymes from solvent-tolerant microbes: Useful biocatalysts for non-aqueous enzymology. Crit Rev Biotechnol 2009, 29:44-54.
• [109]Doukyua N, Ogino H: Organic solvent-tolerant enzymes. Biochem Eng J 2010, 48:270-282.
• [110]Klibanov AM: Why are enzymes less active in organic solvents than in water? Trends Biotechnol 1997, 15:97-101.
• [111]Zhu X, Zhou T, Wu X, Cai Y, Yao D, Xie C, Liu D: Covalent immobilization of enzymes within micro-aqueous organic media. J Mol Catal B: Enzym 2011, 72:145-149.
• [112]Ru MT, Dordick JS, Reimer JA, Clark DS: Optimizing the salt-induced activation of enzymes in organic solvents: Effects of lyophilization time and water content. Biotechnol Bioeng 1999, 63:233-241.
• [113]Torres S, Castro GR: Non-aqueous biocatalysis in homogeneous solvent systems. Food Technol Biotechnol 2004, 42:271-277.
• [114]Gupta MN, Roy I: Enzymes in organic media. Forms, functions and applications. Eur J Biochem 2004, 13:2575-2583.
• [115]Gupta MN: Enzyme function in organic solvents. Eur J Biochem 1992, 203:25-32.
• [116]Ogino H, Uchiho T, Yokoo J, Kobayashi R, Ichise R, Ishikawa H: Role of intermolecular disulfide bonds of the organic solvent-stable PST-01 protease in its organic solvent stability. Appl Environ Microbiol 2001, 67:942-947.
• [117]Ogino H, Uchiho T, Doukyu N, Yasuda M, Ishimi K, Ishikawa H: Effect of exchange amino acid residues of the surface region of the PST-01 protease on its organic solvent-stability. Biochem Biophys Res Commun 2007, 358:1028-1033.
• [118]Gupta A, Ray S, Kapoor S, Khare SK: Solvent-stable Pseudomonas aeruginosa PseA protease gene: identification, molecular characterization, phylogenetic and bioinformatic analysis to study reasons for solvent stability. J Mol Microbiol Biotechnol 2008, 15:234-243.
• [119]Karabec M, Łyskowski A, Tauber KC, Steinkellner G, Kroutil W, Grogan G, Gruber K: Structural insights into substrate specificity and solvent tolerance in alcohol dehydrogenase ADH-'A' from Rhodococcus ruber DSM 44541. Chem Commun (Camb) 2010, 34:6314-6316.
• [120]Rich JO, Dordick JS: Imprinting enzymes for use in organic media. In Enzymes in Nonaqueous Media. Edited by Vulfson J, Halling PJ, Holland HL. Humana Press: Totowa, NJ; 2000.
• [121]Rich JO, Mozhaev VV, Dordick JS, Clark DS, Khmelnitsky YL: Molecular imprinting of enzymes with water-insoluble ligands for nonaqueous biocatalysis. J Am Chem Soc 2002, 124:5254-5255.
• [122]Khmelnitsky Y: Biotransformations in organic chemistry. A textbook, third edition, by Faber K, Springer-Verlag, Berlin; 1997.
• [123]Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE: The Protein Data Bank. Nucleic Acids Res 2000, 28:235-242.
• [124]Guex N, Peitsch MC: SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis 1997, 18:2714-2723.
• [125]Premkumar L, Greenblatt HM, Bageshwar UK, Savchenko T, Gokhman I, Sussman JL, Zamir A: Three-dimensional structure of a halotolerant algal carbonic anhydrase predicts halotolerance of a mammalian homolog. Proc Natl Acad Sci USA 2005, 21:7493-7498.
• [126]Evilia C, Ming X, DasSarma S, Hou YM: Aminoacylation of an unusual tRNA(Cys) from an extreme halophile. RNA 2003, 7:794-801.
• [127]Bohm G, Jaenicke R: A structure-based model for the halophilic adaptation of dihydrofolate reductase from Halobacterium volcanii. Protein Eng 1994, 7:213-220.
• [128]Poidevin L, MacNeill SA: Biochemical characterisation of LigN, an NAD+-dependent DNA ligase from the halophilic euryarchaeon Haloferax volcanii that displays maximal in vitro activity at high salt concentrations. BMC Mol Biol 2006, 7:44.
• [129]Bandyopadhyay AK, Krishnamoorthy G, Padhy LC, Sonawat HM: Kinetics of salt-dependent unfolding of [2Fe-2S] ferredoxin of Halobacterium salinarum. Extremophiles 2007, 4:615-625.
• [130]Britton KL, Stillman TJ, Yip KSP, Forterre P, Engel PC, Rice DW: Insights into the molecular basis of salt tolerance from the study of glutamate dehydrogenase from Halobacterium salinarum. J Biol Chem 1998, 273:9023-9030.
• [131]Chantawannakul P, Yoshimune K, Shirakihara Y, Shiratori A, Wakayama M, Moriguchi M: Crystallization and preliminary X-ray crystallographic studies of salt-tolerant glutaminase from Micrococcus luteus K-3. Acta Crystallogr D Biol Crystallogr 2003, 3:566-568.
• [132]Mevarech M, Eisenberg H, Neumann E: Malate dehydrogenase isolated from extremely halophilic bacteria of the Dead Sea. 1. Purification and molecular characterization. Biochemistry 1977, 17:3781-3785.
• [133]Bonnete ÂF, Madern D, Zaccaõ ÈG: Stability against denaturation mechanisms in halophilic malate dehydrogenase ''adapt'' to solvent conditions. J Mol Biol 1994, 244:436-447.
• [134]Madern D, Pfister C, Zaccai G: Mutation at a single acidic amino acid enhances the halophilic behaviour of malate dehydrogenase from Haloarcula marismortui in physiological salts. Eur J Biochem 1995, 3:1088-1095.
• [135]Richard SB, Madern D, Garcin E, Zaccai G: Halophilic adaptation: novel solvent protein interactions observed in the 2.9 and 2.6 Å resolution structures of the wild type and a mutant of malate dehydrogenase from Haloarcula marismortui. Biochemistry 2000, 5:992-1000.
• [136]Madern D, Zaccai G: Molecular adaptation: the malate dehydrogenase from the extreme halophilic bacterium Salinibacter ruber behaves like a non-halophilic protein. Biochimie 2004, 86:295-303.
• [137]Tehei M, Zaccai G: Adaptation to extreme environments: macromolecular dynamics in complex systems. Biochim Biophys Acta 2005, 3:404-410.
• [138]Manikandan K, Bhardwaj A, Gupta N, Lokanath NK, Ghosh A, Reddy VS, Ramakumar S: Crystal structures of native and xylosaccharide-bound alkali thermostable xylanase from an alkalophilic Bacillus sp. NG-27: structural insights into alkalophilicity and implications for adaptation to polyextreme conditions. Protein Sci 2006, 8:1951-1960.
• [139]Davlieva M, Shamoo 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, 8:751-756.
• [140]Asgeirsson B, Hauksson JB, Gunnarsson GH: Dissociation and unfolding of cold-active alkaline phosphatase from atlantic cod in the presence of guanidinium chloride. Eur J Biochem 2000, 21:6403-6412.
• [141]Tsigos I, Mavromatis K, Tzanodaskalaki M, Pozidis C, Kokkinidis M, Bouriotis V: Engineering the properties of a cold active enzyme through rational redesign of the active site. Eur J Biochem 2001, 268:5074-5080.
• [142]Gudjónsdóttir K, Asgeirsson B: Effects of replacing active site residues in a cold-active alkaline phosphatase with those found in its mesophilic counterpart from Escherichia coli. FEBS J 2008, 1:117-127.
• [143]Bauvois C, Jacquamet L, Huston AL, Borel F, Feller G, Ferrer JL: Crystal structure of the cold-active aminopeptidase from Colwellia psychrerythraea, a close structural homologue of the human bifunctional leukotriene A4 hydrolase. J Biol Chem 2008, 34:23315-23325.
• [144]Huston AL, Haeggström JZ, Feller G: 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 2008, 11:1865-1872.
• [145]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.
• [146]Siddiqui KS, Poljak A, Guilhaus M, Feller G, D'Amico S, Gerday C, Cavicchioli R: Role of disulfide bridges in the activity and stability of a cold-active alpha-amylase. J Bacteriol 2005, 17:6206-6212.
• [147]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, 9:e24214.
• [148]Birolo L, Tutino ML, Fontanella B, Gerday C, Mainolfi K, Pascarella S, Sannia G, Vinci F, Marino G: Aspartate aminotransferase from the Antarctic bacterium Pseudoalteromonas haloplanktis TAC 125. Cloning, expression, properties, and molecular modelling. Eur J Biochem 2000, 9:2790-2802.
• [149]Skálová T, Dohnálek J, Spiwok V, Lipovová P, Vondrácková E, Petroková H, Dusková J, Strnad H, Králová B, Hasek J: Cold-active beta-galactosidase from Arthrobacter sp. C2-2 forms compact 660 kDa hexamers: crystal structure at 1.9Å resolution. J Mol Biol 2005, 2:282-294.
• [150]Lorentzen MS, Moe E, Jouve HM, Willassen NP: Cold adapted features of Vibrio salmonicida catalase: characterisation and comparison to the mesophilic counterpart from Proteus mirabilis. Extremophiles 2006, 5:427-440.
• [151]Riise EK, Lorentzen MS, Helland R, Smalås AO, Leiros HK, Willassen NP: The first structure of a cold-active catalase from Vibrio salmonicida at 1.96 Å reveals structural aspects of cold adaptation. Acta Crystallogr D Biol Crystallogr 2007, 2:135-148.
• [152]Lonhienne T, Zoidakis J, Vorgias CE, 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.
• [153]Russell RJ, Gerike U, Danson MJ, Hough DW, Taylor GL: Structural adaptations of the cold-active citrate synthase from an Antarctic bacterium. Structure 1998, 6:351-361.
• [154]Gerike U, Danson MJ, Hough DW: Cold-active citrate synthase: mutagenesis of active-site residues. Protein Eng 2001, 14:655-661.
• [155]Bell GS, Russell RJM, Connaris H, Hough DW, Danson MJ, Taylor GL: Stepwise adaptations of citrate synthase to survival at life's extremes from psychrophile to hyperthermophile. Eur J Biochem 2002, 269:6250-6260.
• [156]Kumar S, Nussinov R: Different roles of electrostatics in heat and in cold: Adaptation by citrate synthase. Chem Bio Chem 2004, 5:280-290.
• [157]Jung SK, Jeong DG, Lee MS, Lee JK, Kim HK, Ryu SE, Park BC, Kim JH, Kim SJ: Structural basis for the cold adaptation of psychrophilic M37 lipase from Photobacterium lipolyticum. Proteins 2008, 1:476-484.
• [158]Simpson PJ, Codd R: Cold adaptation of the mononuclear molybdoenzyme periplasmic nitrate reductase from the Antarctic bacterium Shewanella gelidimarina. Biochem Biophys Res Commun 2011, 4:783-788.
• [159]Carginale V, Trinchella F, Capasso C, Scudiero R, Parisi E: Gene amplification and cold adaptation of pepsin in Antarctic fish. A possible strategy for food digestion at low temperature. Gene 2004, 2:195-205.
• [160]Miyazaki K, Wintrode PL, Grayling RA, Rubingh DN, Arnold FH: Directed evolution study of temperature adaptation in a psychrophilic enzyme. J Mol Biol 2000, 297:1015-1026.
• [161]Aghajari N, Van Petegem F, Villeret V, Chessa JP, 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.
• [162]Xie BB, Bian F, Chen XL, He HL, Guo J, Gao X, Zeng YX, Chen B, Zhou BC, Zhang YZ: 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 2009, 14:9257-9269.
• [163]Zhong CQ, Song S, Fang N, Liang X, Zhu H, Tang XF, Tang B: Improvement of low-temperature caseinolytic activity of a thermophilic subtilase by directed evolution and site-directed mutagenesis. Biotechnol Bioeng 2009, 5:862-870.
• [164]Sigurdardóttir AG, Arnórsdóttir J, Thorbjarnardóttir SH, Eggertsson G, Suhre K, Kristjánsson MM: Characteristics of mutants designed to incorporate a new ion pair into the structure of a cold adapted subtilisin-like serine proteinase. Biochim Biophys Acta 2009, 3:512-518.
• [165]Almog O, González A, Godin N, de Leeuw M, Mekel MJ, Klein D, Braun S, Shoham G, Walter RL: The crystal structures of the psychrophilic subtilisin S41 and the mesophilic subtilisin Sph reveal the same calcium-loaded state. Proteins 2009, 2:489-496.
• [166]Karan R, Khare SK: Stability of haloalkaliphilic Geomicrobium sp. protease modulated by salt. Biochemistry (Mosc) 2011, 76:686-693.
• [167]Karan R, Singh RK, Kapoor S, Khare SK: Gene identification and molecular characterization of solvent stable protease from a moderately haloalkaliphilic bacterium, Geomicrobium sp. EMB2. J Microbiol Biotechnol 2011, 2:129-135.
• [168]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 2001, 12:975-982.
• [169]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 1997, 10:1271-1279.
• [170]Matsumoto M, Yokouchi H, Suzuki N, Ohata H, Matsunaga T: Saccharification of marine microalgae using marine bacteria for ethanol production. Appl Biochem Biotechnol 2003, 108:247-254.
• [171]Fukushima T, Mizuki T, Echigo A, Inoue A, Usami R: Organic solvent tolerance of halophilic α-amylase from a Haloarchaeon, Haloarcula sp. strain S-1. Extremophiles 2005, 9:85-89.
• [172]Chakraborty S, Khopade A, Kokare C, Mahadik K, Chopade B: Isolation and characterization of novel a-amylase from marine Streptomyces sp. D1. J Mol Catalysis B Enzymatic 2009, 58:17-23.
• [173]Kosjek B, Stampfer W, Pogorevc M, Goessler W, Faber K, Kroutil W: Purification and characterization of a chemotolerant alcohol dehydrogenase applicable to coupled redox reactions. Biotechnol Bioeng 2004, 86:55-62.
• [174]Kobori H, Sullivan CW, Shizuya H: Heat-labile alkaline phosphatase from antarctic bacteria: rapid 5' end-labeling of nucleic acids. Proc Natl Acad Sci USA 1984, 81:6691-6695.
• [175]Hoyoux A, Jennes I, Dubois P, Genicot S, Dubail F, François JM, Baise E, Feller G, Gerday C: Cold-adapted beta-galactosidase from the Antarctic psychrophile Pseudoalteromonas haloplanktis. Appl Environ Microbiol 2001, 67:1529-1535.
• [176]Maugard T, Gaunt D, Legoy MD, Besson T: Microwave-assisted synthesis of galacto-oligosaccharides from lactose with immobilized beta-galactosidase from Kluyveromyces lactis. Biotechnol Lett 2003, 25:623-629.
• [177]Hildebrandt P, Wanarska M, Kur J: A new cold-adapted β-D-galactosidase from the Antarctic Arthrobacter sp. 32c- gene cloning, overexpression, purification and properties. BMC Microbiology 2009, 9:151.
• [178]Bridiau N, Issaoui N, Maugard T: The effects of organic solvents on the efficiency and regioselectivity of N-acetyl-lactosamine synthesis, using the β-galactosidase from Bacillus circulans in hydro-organic media. Biotechnol Prog 2010, 26:1278-1289.
• [179]Hatori Y, Sato M, Orishimo K, Yatsunami R, Endo K, Fukui T, Nakamura S: Characterization of recombinant family 18 chitinase from extremely halophilic archaeon Halobacterium salinarum strain NRC-1. Chitin Chitosan Res 2006, 12:201.
• [180]Essghaier B, Hedi A, Bejji M, Jijakli H, Boudabous A, Sadfi-Zouaoui N: Characterization of a novel chitinase from a moderately halophilic bacterium, Virgibacillus marismortui strain M3-23. Annal Microbiol 2011. DOI: 10.1007/s13213-011-0324-4
• [181]Doukyu N, Aono R: Purification of extracellular cholesterol oxidase with high activity in the presence of organic solvents from Pseudomonas sp ST-200. Appl Environ Microbiol 1998, 64:1929-1932.
• [182]Yoshimune K, Shirakihara Y, Wakayama M, Yumoto I: Crystal structure of salt-tolerant glutaminase from Micrococcus luteus K-3 in the presence and absence of its product L-glutamate and its activator Tris. FEBS J 2010, 3:738-748.
• [183]Hotta Y, Ezaki S, Atomi H, Imanaka T: Extremely stable and versatile carboxyl esterase from a hyperthermophilic archaeon. Appl Environ Microbiol 2002, 68:3925-3931.
• [184]Khudary RA, Venkatachalam R, Katzer M, Elleuche S, Antranikian G: A cold-adapted esterase of a novel marine isolate, Pseudoalteromonas arctica: gene cloning, enzyme purification and characterization. Extremophiles 2010, 14:273-285.
• [185]Kirk O, Christensen MW: Lipases from Candida antarctica: Unique biocatalysts from a unique origin. Org Process Res Dev 2002, 6:446-451.
• [186]Giudice AL, Michaud L, de Pascale D, Domenico MD, di Prisco G, Fani R, Bruni V: Lipolytic activity of Antarctic cold adapted marine bacteria. J Appl Microbiol 2006, 101:1039-1048.
• [187]Joseph B, Ramteke PW, Kumar PA: Studies on the enhanced production of extracellular lipase by Staphylococcus epidermidis. J Gen Appl Microbiol 2006, 52:315-320.
• [188]Amoozegar MA, Salehghamari E, Khajeh K, Kabiri M, Naddaf S: Production of an extracellular thermohalophilic lipase from a moderately halophilic bacterium, Salinivibrio sp. strain SA-2. J Basic Microbiol 2008, 48:160-167.
• [189]Gaur R, Gupta A, Khare SK: Purification and characterization of lipase from solvent tolerant Pseudomonas aeruginosa PseA. Process Biochem 2008, 43:1040-1046.
• [190]Pérez D, Martín S, Fernández-Lorente G, Filice M, Guisán JM, Ventosa A, García MT, Mellado E: A novel halophilic lipase, LipBL, showing high efficiency in the production of eicosapentaenoic acid (EPA). PLoS ONE 2011, 6:e23325.
• [191]Kamekura M, Hamakawa T, Onishi H: Application of halophilic nuclease H of Micrococcus varians subsp. halophilus to commercial production of flavoring agent 5'-GMP. Appl Environ Microbiol 1982, 44:994-995.
• [192]Truong LV, Tuyen H, Helmke E, Binh LT, Schweder T: Cloning of two pectate lyase genes from the marine Antarctic bacterium Pseudoalteromonas haloplanktis strain ANT/505 and characterization of the enzymes. Extremophiles 2001, 5:35-44.
• [193]Ryu K, Kim J, Dordick JS: Catalytic properties and potential of an extracellular protease from an extreme halophile. Enzym Microb Technol 1994, 16:266-275.
• [194]Kim J, Dordick JS: Unusual salt and solvent dependence of a protease from an extreme halophile. Biotechnol Bioeng 1997, 55:471-479.
• [195]Bobe IM, Abdelmoez W, Ogino H, Yasuda M, Ishimi K, Ishikawa H: Kinetics and mechanism of a reaction catalyzed by PST-01 protease from Pseudomonas aeruginosa PST-01. Biotechnol Bioeng 2004, 86:365-373.
• [196]Tsuchiyama S, Doukyu N, Yasuda M, Ishimi K, Ogino H: Peptide synthesis of aspartame precursor using organic solvent-stable PST-01 protease in monophasic aqueous organic solvent systems. Biotechnol Prog 2007, 23:820-823.
• [197]Gupta A, Roy I, Khare SK, Gupta MN: Purification and characterization of a solvent stable protease from Pseudomonas aeruginosa PseA. J Chrom A 2005, 1069:155-161.
• [198]Pawar R, Zambare V, Barve S, Paratkar G: Application of protease isolated from Bacillus sp. in enzymatic cleansing of contact lenses. Biotechnol 2009, 8:276-280.
• [199]Ruiz DM, Iannuci NB, Cascone O, De Castro RE: Peptide synthesis catalysed by a haloalkaliphilic serine protease from the archaeon Natrialba magadii (Nep). Lett Appl Microbiol 2010, 51:691-696.
• [200]Akolkar AV, Durai D, Desai AJ: Halobacterium sp. SP1 (1) as a starter culture for accelerating fish sauce fermentation. J Appl Microbiol 2010, 109:44-53.
• [201]Karan R, Khare SK: Purification and characterization of a solvent stable protease from Geomicrobium sp EMB2. Environ Technol 2010, 10:1061-1072.
• [202]Karan R, Singh SP, Kapoor S, Khare SK: A novel organic solvent tolerant protease from a newly isolated Geomicrobium sp. EMB2 (MTCC 10310): production optimization by response surface methodology. N Biotechnol 2011, 2:136-145.
• [203]Collins T, Hoyoux A, Dutron A, Georis J, Genot B, Dauvrin T, Arnaut F, Gerday C, Feller G: Use of glycoside hydrolase family 8 xylanases in baking. J Cereal Sci 2006, 43:79-84.
• [204]Dornez E, Verjans P, Arnaut F, Delcour JA, Courtin CM: Use of psychrophilic xylanases provides insight into the xylanase functionality in bread making. J Agric Food Chem 2011, 17:9553-9562.
• [205]Wang K, Li G, Yu SQ, Zhang CT, Liu YH: A novel metagenome-derived beta-galactosidase: gene cloning, overexpression, purification and characterization. Appl Microbiol Biotechnol 2010, 88:155-165.
• [206]Prakash P, Jayalakshmi SK, Prakash B, Rubul M, Sreeramulu K: Production of alkaliphilic, halotolerent, thermostable cellulase free xylanase by Bacillus halodurans PPKS-2 using agro waste: single step purification and characterization. World J Microbiol Biotechnol 2011. DOI: 10.1007/s11274-011-0807-2