Extremozymes: A Potential Source for Industrial Applications

Kelly  Dumorné; David Camacho  Córdova; Marcia  Astorga-Eló; Prabhaharan  Renganathan

doi:10.4014/jmb.1611.11006

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Biotechnology and Bioengineering (BB) | Enzyme, Protein Engineering, and Metabolic Engineering

Extremozymes: A Potential Source for Industrial Applications

Kelly Dumorné ^1*, David Camacho Córdova ², Marcia Astorga-Eló ³ and Prabhaharan Renganathan ⁴

¹Departamento de Ingeniería Química, Facultad de Ciencias Químicas y Recursos Naturales, Universidad de La Frontera, Chile, ¹Department of Pharmaceutical Sciences, Faculty of Pharmaceutical Sciences of Ribeirao Preto, University of Sao Paulo-USP, Brazil, ²Department of Food Technology, University of Sonora, Mexico, ³Laboratorio Ecología Microbiana Aplicada, Departamento de Ingeniería Química, Facultad de Ciencias Químicas y Recursos Naturales,Universidad de La Frontera, Chile

Received: November 3, 2016; Accepted: January 19, 2017

J. Microbiol. Biotechnol. 2017; 27(4): 649-659

Published April 28, 2017 https://doi.org/10.4014/jmb.1611.11006

Abstract

Extremophilic microorganisms have established a diversity of molecular strategies in order to survive in extreme conditions. Biocatalysts isolated by these organisms are termed extremozymes, and possess extraordinary properties of salt allowance, thermostability, and cold adaptivity. Extremozymes are very resistant to extreme conditions owing to their great solidity, and they pose new opportunities for biocatalysis and biotransformations, as well as for the development of the economy and new line of research, through their application. Thermophilic proteins, piezophilic proteins, acidophilic proteins, and halophilic proteins have been studied during the last few years. Amylases, proteases, lipases, pullulanases, cellulases, chitinases, xylanases, pectinases, isomerases, esterases, and dehydrogenases have great potential application for biotechnology, such as in agricultural, chemical, biomedical, and biotechnological processes. The study of extremozymes and their main applications have emerged during recent years.

Keywords

Extremozymes, thermophiles, acidophiles, halophiles, biotechnology

References

Cavicchioli R, Amils D, McGenity T. 2011. Life and applications of extremophiles. Environ. Microbiol. 13: 19031907.
Deppe U, Richnow HH, Michaelis W, Antranikian G. 2005. Degradation of crude oil by an arctic microbial consortium. Extremophiles 9: 461-470.
Navarro-González R, Iniguez E, de la Rosa J, McKay CR. 2009. Characterization of organics, microorganisms, desert soil, and Mars-like soils by thermal volatilization coupled to mass spectrometry and their implications for the search for organics on Mars by Phoenix and future space missions. Astrobiology 9: 703-711.
Seitz KH, Studdert C, Sanchez J, de Castro R. 1997. Intracellular proteolytic activity of the haloalkaliphilic archaeon Natronococcus occultus. Effect of starvation. J. Basic Microbiol. 7: 313-322.
Cárdenas JP, Valdés J, Quatrini R, Duarte F, Holmes DS. 2010. Lessons from the genomes of extremely acidophilic bacteria and archaea with special emphasis on bioleaching microorganisms. Appl. Microbiol. Biotechnol. 88: 605-620.
López-López O, Cerdán ME, González-Siso MI. 2014. New extremophilic lipases and esterases from metagenomics. Curr. Protein Pept. Sci. 15: 445-455.
Yildiz SY, Radchenkova N, Arga KY, Kambourova M, Toksoy OE. 2015. Genomic analysis of Brevibacillus thermoruber 423 reveals its biotechnological and industrial potential. Appl. Microbiol. Biotechnol. 99: 2277-2289.
Cowan DA, Ramond JB, Makhalanyane TP, De Maayer P. 2015. Metagenomics of extreme environments. Curr. Opin. Microbiol. 25: 97-102.
Qin J, Zhao B, Wang X. 2009. Non-sterilized fermentative production of polymer-grade L-lactic acid by a newly isolated thermophilic strain Bacillus sp. PLoS One 4: 43-59.
Karan R, Capes MD, DasSarma S. 2012. Function and biotechnology of extremophilic enzymes in low water activity. Aquat. Biosyst. 8: 3-15.
Nigam SP. 2013. Microbial enzymes with special characteristics for biotechnological applications. Biomolecules 3: 597-611.
Singh OV, Gabani P. 2011. Extremophiles: radiation resistance microbial reserves and therapeutic implications. J. Appl. Microbiol. 110: 851-861.
Demirjian DC, Morís-Varas F, Cassidy CS. 2001. Enzymes from extremophiles. Curr. Opin. Chem. Biol. 5: 144-151.
Van den Burg B. 2003. Extremophiles as a source for novel enzymes. Curr. Opin. Microbiol. 6: 213-218.
Irwin JA, Baird AW. 2004. Extremophiles and their application to veterinary medicine. Ir. Vet. J. 57: 348-354.
Díaz-Tenaa E, Rodríguez-Ezquerroa A, López de Lacalle Marcaide LN, Bustinduyb LG, Sáenzb AE. 2013. Use of extremophiles microorganisms for metal removal. Procedia Eng. 63: 67-74.
Eichler J. 2001. Biotechnological uses of archaeal extremozymes. Biotechnol. Adv. 19: 261-278.
Fujiwara S. 2002. Extremophiles: developments of their special functions and potential resources. J. Biosci. Bioeng. 94: 518-525.
Haki GD, Rakshit SK. 2003. Developments in industrially important thermostable enzymes: a review. Bioresour. Technol. 89: 7-34.
Raddadi N, Cherif A, Daffonchio D, Mohamed N, Fava F. 2015. Biotechnological applications of extremophiles, extremozymes and extremolytes. Appl. Microbiol. Biotechnol. 99: 7907-7913.
Dewan S. 2014. Global Markets for Enzymes in Industrial Applications. BCC Research, Wellesley, MA. USA.
Marhuenda-Egea FC, Piere-Velazquez S, Cadenas C, Cadenas E. 2002. An extreme halophilic enzyme active at low salt in reversed micelles. J. Biotechnol. 93: 159-164.
Jaenicke R, Schuring H, Beaucamp N, Ostendorp R. 1996. Structure and stability of hyperstable proteins: glycolytic enzymes from hyperthermophilic bacterium Thermotoga maritima. Adv. Protein Chem. 48: 181-269.
Sthal S. 1993. In Gupta MN (ed.). Thermostability of Enzymes, pp. 45-74. Springer, Berlin, Germany.
Cavicchioli R, Siddiqui KS, Andrews D, Sowers KR. 2002. Low-temperature extremophiles and their applications. Curr. Opin. Biotechnol. 13: 253-261.
Bertoldo C, Antranikian G. 2002. Starch-hydrolyzing enzymes from thermophilic archaea and bacteria. Curr. Opin. Chem. Biol. 6: 151-60.
Van der Maarel MJ, van der Veen B, Uitdehaag JC, Leemhuis H, Dijkhuizen L. 2002. Properties and application of starch-converting enzymes of the α-amylase family. J. Biotechnol. 94: 137-155.
Madigan MT, Marrs BL. 1997. Gli estremofili. Le Scienze 346: 78-85.
Sunna A, Bergquist PL. 2003. A gene encoding a novel extremely thermostable 1,4-beta-xylanase isolated directly from an environmental DNA sample. Extremophiles 7: 63-70.
Brasen C, Urbanke C, Schonheit P. 2005. A novel octameric AMP-forming acetyl-CoA synthetase from the hyperthermophilic crenarchaeon Pyrobaculum aerophilum. FEBS Lett. 579: 477482.
Mayer F, Küper U, Meyer C, Daxer S, Müller V, Rachel R, Huber H. 2012. AMP-forming acetyl coenzyme A synthetase in the outermost membrane of the hyperthermophilic crenarchaeon Ignicoccus hospitalis. J. Bacteriol. 194: 1572-1581.
Staiano M, Bazzicalupo P, Rossi M, D’Auria S. 2005. Glucose biosensors as models for the development of advanced protein-based biosensors. Mol. Biosyst. 1: 354-362.
Bruins ME, Janssen AE, Boom RM. 2001. Thermozymes and their applications: a review of recent literature and patents. Appl. Biochem. Biotechnol. 90: 155-186.
Jayakumar R, Jayashree S, Annapurna B, Seshadri S. 2012. Characterization of thermostable serine alkaline protease from an alkaliphilic strain Bacillus pumilus MCAS8 and its applications. Appl. Biochem. Biotechnol. 168: 1849-1866.
De Pascale D, Cusano AM, Author F, Parrilli E, di Prisco G, Marino G, Tutino ML. 2008. The cold-active Lip1 lipase from the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125 is a member of a new bacterial lipolytic enzyme family. Extremophiles 12: 311-323.
Unsworth LD, Van Der OJ, Koutsopoulos S. 2007. Hyperthermophilic enzymes - stability, activity and implementation strategies for high temperature applications. FEBS J. 274:4044-4056.
Rosenbaum E, Gabel F, Durá MA, Finet S, Cléry-Barraud C, Masson P, Franzetti B. 2012. Effects of hydrostatic pressure on the quaternary structure and enzymatic activity of a large peptidase complex from Pyrococcus horikoshii. Arch. Biochem. Biophys. 517: 104-110.
De Champdoré M, Staiano M, D’Auria S. 2007. Proteins from extremophiles as stable tools for advanced biotechnological applications of high social interest. J. R. Soc. Interface 4:183-191.
Boonyaratanakornkit BB, Park CB, Clark DS. 2002. Pressure effects on intra- and intermolecular interactions within proteins. Biochim. Biophys. Acta 1595: 235-249.
Fang J, Zhang L, Bazylinski DA. 2010. Deep-sea piezosphere and piezophiles: geomicrobiology and biogeochemistry. Trends Microbiol. 18: 413-422.
Reed CJ, Lewis H, Trejo E, Winston V, Evilia C. 2013. Protein adaptations in archaeal extremophiles. Archaea 2013: 373275.
Simonato F, Campanaro S, Lauro FM, Vezzi A, D’Angelo M, Vitulo N. 2006. Piezophilic adaptation: a genomic point of view. J. Biotechnol. 126: 11-25.
Takai K, Miyazaki M, Hirayama H, Nakagawa S, Querellou J, Godfroy A. 2009. Isolation and physiological characterization of two novel piezophilic, thermophilic chemolithoautotrophs from a deep-sea hydrothermal vent chimney. Environ. Micriobiol. 11: 1983-1997.
Fusi P, Grisa M, Mombelli E, Consonni R, Tortora P, Vanoni M. 1995. Expression of a synthetic gene encoding P2 ribonuclease from the extreme thermoacidophilic archaebacterium Sulfolobus solfataricus in mesophylic hosts. Gene 154: 99-103
Mombelli E, Shehi E, Fusi P, Tortora P. 2002. Exploring hyperthermophilic proteins under pressure: theoretical aspects and experimental findings. Biochim. Biophys. Acta 1595: 392-396.
Cavicchioli R. 2002. Extremophiles and the search for extraterrestrial life. Astrobiology 2: 281-292.
Georlette D, Blaise V, Collins T, D’Amico S, Gratia E, Hoyoux A, et al. 2004. Some like it cold: biocatalysis at low temperatures. FEMS Microbiol. Rev. 28: 25-42.
Gomes J, Steiner W. 1998. Production of a high activity of an extremely thermostable β-mannanase by the thermophilic eubacterium Rhodothermus marinus. Biotechnol. Lett. 20: 729733.
Gomes J, Gomes I, Terler K, Gubala N, Ditzelmuller G, Steiner W. 2000. Optimisation of culture medium and conditions for α-L-arabinofuranosidase production by the extreme thermophilic eubacterium Rhodothermus marinus. Enzyme Microb. Technol. 27: 414-422.
Abe F, Horikoshi K. 2001. The biotechnological potential of piezophiles. Trends Biotechnol. 19: 102-108.
Cannio R, Di Prizito N, Rossi M, Morana A. 2004. A xylandegrading strain of Sulfolobus solfataricus: isolation and characterization of the xylanase activity. Extremophiles 8:117-124.
Giuliano M, Schiraldi C, Marotta MR, Hugenholtz J, De Rosa M. 2004. Expression of Sulfolobus solfataricus αglucosidase in Lactococcus lactis. Appl. Microbiol. Biotechnol. 64: 829-832.
Jaenicke R. 1981. Enzymes under extreme of physical conditions. Annu. Rev. Biophys. Bioeng. 10: 1-67.
Huang Y, Krauss G, Cottaz H, Driguez H, Lipps G. 2005. A highly acid-stable and thermostable endo-β-glucanase from the thermoacidophilic archaeon Sulfolobus solfataricus. Biochem. J. 385: 581-588.
Golyshina O, Timmis KN. 2005. Ferroplasma and relatives, recently discovered cell wall-lacking archaea making a living in extremely acid, heavy metal-rich environments. Environ. Microbiol. 7: 1277-1288.
Sharma A, Kawarabayasi Y, Satyanarayana T. 2012. Acidophilic bacteria and archaea: acid stable biocatalysts and their potential applications. Extremophiles 16: 1-19.
Pikuta EV, Hoover RB, Tang J. 2007. Microbial extremophiles at the limits of life. Crit. Rev. Microbiol. 33: 183-209.
Hauenstein S, Zhang CM, Hou YM, Perona JJ. 2004. Shapeselective RNA recognition by cysteinyl-tRNA synthetase. Nat. Struct. Mol. Biol. 11: 1134-1141.
Szilágyi A, Závodszky P. 2000. Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Structure 8: 493-504.
Wright DB, Banks DD, Lohman JR, Hilsenbeck JL, Gloss LM. 2002. The effect of salts on the activity and stability of Escherichia coli and Haloferax volcanii dihydrofolate reductases. J. Mol. Biol. 323: 327-344.
Jackson BR, Noble C, Lavesa-Curto M, Bond PL, Bowater RP. 2007. Characterization of an ATP-dependent DNA ligase from the acidophilic archaeon “Ferroplasma acidarmanus” Fer1. Extremophiles 11: 315-327.
Delgado-García M, Valdivia-Urdiales B, Aguilar-González CN, Contreras-Esquivel JC, Rodríguez-Herrera R. 2012. Halophilic hydrolases as a new tool for the biotechnological industries. J. Sci. Food Agric. 92: 2575-2580.
Jackson CR, Langner HW, Donahoe-Christiansen J, Inskeep WP, McDermott TR. 2001. Molecular analysis of microbial community structure in an arsenite-oxidizing acidic thermal spring. Environ. Microbiol. 3: 532-542.
Datta S, Holmes B, Park J, Chen Z, Dibble DC, Hadi M, et al. 2010. Ionic liquid tolerant hyperthermophilic cellulases for biomass pretreatment and hydrolysis. Green Chem. 12: 338345.
Madern D, Pfister C, Zaccai G. 1995. Mutation at a single acidic amino acid enhances the halophilic behaviour of malate dehydrogenase from Haloarcula marismortui in physiological salts. Eur. J. Biochem. 3: 1088-1095.
Raddadi N, Cherif A, Daffonchio D, Fava F. 2013. Haloalkalitolerant and thermostable cellulases with improved tolerance to ionic liquids and organic solvents from Paenibacillus tarimensis isolated from the Chott El Fejej, Sahara desert, Tunisia. Bioresour. Technol. 150: 121-128.
Bhalla A, Bansal N, Kumar S, Bischoff KM, Sani RK. 2013. Improved lignocellulose conversion to biofuels with thermophilic bacteria and thermostable enzymes. Bioresour. Technol. 128: 751-759.
Elleuche S, Schröder C, Sahm K, Antranikian G. 2014. Extremozymes - biocatalysts with unique properties from extremophilic microorganisms. Curr. Opin. Biotechnol. 29:116-123.
Madern D, Ebel C, Zaccai G. 2000. Halophilic adaptation of enzymes. Extremophiles 4: 91-98.
Sutrisno A, Ueda M, Abe Y, Nakazawa M, Miyatake K. 2004. A chitinase with high activity toward partially Nacetylated chitosan from a new, moderately thermophilic, chitin-degrading bacterium, Ralstonia sp. A-471. Appl. Microbiol. Biotechnol. 63: 398-406.
Taylor INR, Brown C, Rycroft M, King G, Littlechild JA, Lloyd MC, et al. 2004. Application of thermophilic enzymes in commercial biotransformation processes. Biochem. Soc. Trans. 32: 290-292.
Woosowska S, Synowiecki J. 2004. Thermostable glucosidase with broad substrate specificity suitable for processing of lactose-containing products. Food Chem. 85: 181-187.
Litchfield CD. 2011. Potential for industrial products from the halophilic Archaea. J. Ind. Microbiol. Biotechnol. 38:1635-1647.
Schreck SD, Grunden AM. 2014. Biotechnological applications of halophilic lipases and thioesterases. Appl. Microbiol. Biotechnol. 98: 1011-1021.
Ortega G, Laín A, Tadeo X, López-Méndez B, Castaño D, Milleta O. 2011. Halophilic enzyme activation induced by salts. Sci. Rep. 1: 6.
Serour E, Antranikian G. 2002. Novel thermoactive glucoamylases from the thermoacidophilic Archaea Thermoplasma acidophilum, Picrophilus torridus and Picrophilus oshimae. Antonie Van Leeuwenhoek 81: 73-83.
Suzuki T, Nakayama T, Kurihara T, Nishino T, Esaki N. 2001. Cold-active lipolytic activity of psychrotrophic Acinetobacter sp. strain no. 6. J. Biosci. Bioeng. 92: 144-148.
Kim J, Dordick S. 1997. Unusual salt and solvent dependence of a protease from an extreme halophile. Biotechnol. Bioeng. 55: 471-479.
Karbalaei-Heidari HR, Ziaee AA, Amoozegar MA. 2007. Purification and biochemical characterization of a protease secreted by the Salinivibrio sp. strain AF-2004 and its behavior in organic solvents. Extremophiles 11: 237-243.
Ruiz DM, De Castro RE. 2007. Effect of organic solvents on the activity and stability of an extracellular protease secreted by the haloalkaliphilic archaeon Natrialba magadii. J. Ind. Microbiol. Biotechnol. 34: 111-115.
Fukushima T, Mizuki T, Echigo A, Inoue A, Usami R. 2005. Organic solvent tolerance of halophilic a-amylase from a haloarchaeon, Haloarcula sp. strain S-1. Extremophiles 9: 85-89.
Shafiei M, Ziaee AA, Amoozegar MA. 2011. Purification and characterization of an organic-solvent-tolerant halophilic a-amylase from the moderately halophilic Nesterenkonia sp. strain F. J. Ind. Microbiol. Biotechnol. 38: 275-281.
Yu HY, Li X. 2012. Purification and characterization of novel organic-solvent-tolerant b-amylase and serine protease from a newly isolated Salimicrobium halophilum strain LY20. FEMS Microbiol. Lett 329: 204-211.
Munawar N, Engel PC. 2012. Overexpression in a non-native halophilic host and biotechnological potential of NAD+dependent glutamate dehydrogenase from Halobacterium salinarum strain NRC-36014. Extremophiles 16: 463-476.
Vidyasagar M, Prakash S, Sreeramulu K. 2006. Optimization of culture conditions for the production of haloalkaliphilic thermostable protease from an extremely halophilic archaeon Halogeometricum borinquense sp. TSS 101. Lett. Appl. Microbiol. 43: 385-391.
Zaccai G. 2004. The effect of water on protein dynamics. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359: 1269-1275.
Sellek GA, Chaudhuri JB. 1999. Biocatalysis in organic media using enzymes from extremophiles. Enzyme Microb. Technol. l25: 471-482.
Cordone L, Ferrand M, Vitrano E, Zaccai G. 1999. Harmonic behavior of trehalose-coated carbon-monoxymyoglobin at high temperature. Biophys. J. 76: 1043-1047.
Lehnert U, Réat V, Weik M, Zaccaï G, Pfister C. 1998. Thermal motions in bacteriorhodopsin at different hydration levels studied by neutron scattering: correlation with kinetics and light-induced conformational changes. Biophys. J. 75:1945-1952.
Singh A, Kuhad RC, Ward OP. 2007. Industrial application of microbial cellulases, pp. 345-358. In Kuhad RC, Singh A (eds.). Lignocellulose Biotechnology: Future Prospects. I.K. International Publishing House, New Delhi, India.
Merlino A, Russo KI, Castellano I, De VE, Rossi B, Conte M, et al. 2010. Structure and flexibility in cold-adapted iron superoxide dismutases: the case of the enzyme isolated from Pseudoalteromonas haloplanktis. J. Struct. Biol. 172: 343352.
Siddiqui KS, Cavicchioli R. 2006. Cold-adapted enzymes. Annu. Rev. Biochem. 75: 403-433.
Sukumaran RK, Singhania RR, Pandey A. 2005. Microbial cellulases - production, applications and challenges. J. Sci. Ind. Res. 64: 832-844.
Kumar L, Awasthi G, Singh B. 2011. Extremophiles: a novel source of industrially important enzymes. Biotechnol. Appl. Biochem. 10: 1-15.
Gerday C, Aittaleb M, Bentahir M, Chessa JP, Claverie P, Collins T, et al. 2000. Cold-adapted enzymes: from fundamentals to biotechnology. Trends Biotechnol. 18: 103-107.
Huston AL. 2008. Biotechnological aspects of cold-adapted enzymes, pp. 347-363. In Margesin R, Schinner F, Marx J-C, Gerday C (eds.). Psychrophiles: From Biodiversity to Biotechnology. Springer, Heidelberg. Germany.
Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S, et al. 2012. A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS One 7: e48479.
Rolli E, Marasco M, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, et al. 2015. Improved plant resistance to drought is promoted by the root-associated microbiome as water stress-dependent trait. Environ. Microbiol. 17: 316-331.
Hotta Y, Ezaki S, Atomi H, Imanaka T. 2002. Extremely stable and versatile carboxylesterase from a hyperthermophilic archaeon. Appl. Environ. Microbiol. 68: 3925-3931.
Johnson DB. 2014. Biomining - biotechnologies for extracting and recovering metals from ores and waste materials. Curr. Opin. Biotechnol. 30: 24-31.
Karasová-Lipovová P, Strnad H, Spiwok V, Malá S, Králová B, Russell NJ. 2003. The cloning, purification and characterisation of a cold-active β-galactosidase from the psychrotolerant Antarctic bacterium Arthrobacter sp. C2-2. Enzyme Microb. Technol. 33: 836-844.
Navarro CA, von Bernath D, Jerez CA. 2013. Heavy metal resistance strategies of acidophilic bacteria and their acquisition: importance for biomining and bioremediation. Biol. Res. 46: 363-371.
Adrio JL, Demain AL. 2014. Microbial enzymes: tools for biotechnological processes. Biomolecules 4: 117-139.
Karmakar M, Ray RR. 2011. Current trends in research and application of microbial cellulases. Res. J. Microbiol. 6: 4153.
Birgisson H, Delgado O, Arroyo LG, Hatti-Kaul R, Mattiasson B. 2003. Cold-adapted yeasts as producers of cold-active polygalacturonases. Extremophiles 7: 185-193.
Singh BK. 2010. Exploring microbial diversity for biotechnology:the way forward. Trends Biotechnol. 28: 111-116.
Hess M, Katzer M, Antranikian G. 2008. Extremely thermostable esterases from the thermoacidophilic euryarchaeon Picrophilus torridus. Extremophiles 12: 351-364.
Staley JT, Konopka A. 1985. Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu. Rev. Microbiol. 39: 321-346.
Young P. 1997. Major microbial diversity initiative recommended. ASM News 63: 417-421.
Mohammed K, Pramod WR. 2009. Cold-active extracellular alkaline protease from an alkaliphilic Stenotrophomonas maltophilia: production of enzyme and its industrial applications. Can. J. Microbiol. 55: 1294-1301.
Yumoto I. 2002. Bioenergetics of alkaliphilic Bacillus spp. J. Biosci. Bioeng. 93: 342-353.
Chang P, Tsai WS, Tsai CL, Tseng MJ. 2004. Cloning and characterization of two thermostable xylanases from an alkaliphilic Bacillus firmus. Biochem. Biophys. Res. Commun. 319: 1017-1025.
Das H, Sing SK. 2004. Useful byproducts from cellulosic waste of agriculture and food industry - a critical appraisal. Crit. Rev. Food Sci. Nutr. 44: 77-89.
Hashim SO, Delgado O, Hatti-Kaul R, Mulaa FJ, Mattiasson B. 2004. Starch hydrolysing Bacillus halodurans isolates from a Kenyan soda lake. Biotechnol. Lett. 26: 823-828.
Von Solingen P, Meijer D, Kleij WA, Branett C, Bolle R, Power SD, Jones BE. 2001. Cloning and expression of an endocellulase gene from a novel streptomycete isolated from an East African soda lake. Extremophiles 5: 333-341.
Ma Y, Xue Y, Grant WD, Collins NC, Duckworth AW, Van Steenbergen RP, Jones BE. 2004. Alkalimonas amylolytica gen. nov., sp. nov., and Alkalimonas delamerensis gen. nov., sp. nov., novel alkaliphilic bacteria from soda lakes in China and East Africa. Extremophiles 8: 193-200.
Margesin R, Schinner F, Marx JC, Gerday C (eds.). 2008. Psychrophiles: From Biodiversity to Biotechnology. SpringerVerlag, Berlin-Heidelberg. Germany.
Zeng R, Zhang R, Zhao J, Lin N. 2003. Cold-active serine alkaline protease from the psychrophilic bacterium Pseudomonas strain DY-A: enzyme purification and characterization. Extremophiles 7: 335-337.
Collins T, D’Amico S, Marx JC, Feller G, Gerday C. 2007. Cold-adapted enzymes, pp. 165-179. In Gerday C, Glansdorff N (eds.). Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. USA.
Gurung N, Ray S, Bose S, Rai V. 2013. A broader view:microbial enzymes and their relevance in industries, medicine, and beyond. Biomed. Res. Int. 2013: 329121.
Egorova K, Antranikian G. 2005. Industrial relevance of thermophilic Archaea. Curr. Opin. Microbiol. 8: 649-655.
Ferrer M, Golyshina O, Beloqui A, Golyshin PN. 2007. Mining enzymes from extreme environments. Curr. Opin. Microbiol. 10: 207-214.
Secades P, Alvarez B, Guijarro JA. 2003. Purification and properties of a new psychrophilic metalloprotease (Fpp2) in the fish pathogen Flavobacterium psychrophilum. FEMS Microbiol. Lett. 226: 273-279.
Huang H, Luo H, Wang Y, Fu D, Shao N, Yang P, et al. 2009. Novel low-temperature-active phytase from Erwinia carotovora var. carotovota ACCC 10276. J. Microbiol. Biotechnol. 19: 1085-1091.
Tutino ML, di Prisco G, Marino G, de Pascale D. 2009. Cold-adapted esterases and lipases: from fundamentals to application. Protein Pept. Lett. 16: 1172-1180.
Ueda M, Goto T, Nakazawa M, Miyatake K, Sakaguchi M, Inouye K. 2010. A novel cold-adapted cellulase complex from Eisenia foetida: characterization of a multienzyme complex with carboxymethylcellulase, beta-glucosidase, beta-1,3 glucanase, and beta-xylosidase. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 157: 26-32.
Wang F, Hao J, Yang C, Sun M. 2010. Cloning, expression, and identification of a novel extracellular cold-adapted alkaline protease gene of the marine bacterium strain YS80-122. Appl. Biochem. Biotechnol. 162: 1497-1505.
Parkes R, Cragg J, Banning BA, Brock N, Webster F, Fry G, et al. 2007. Biogeochemistry and biodiversity of methane cycling in subsurface marine sediments (Skagerrak, Denmark). Environ. Microbiol. 9: 1146-1161.
Aurilia V, Parracino A, D’Auria S. 2008. Microbial carbohydrate esterases in cold adapted environments. Gene 410: 234-240.
Toplin JA, Norris TB, Lehr CR, McDermott TR, Castenholz RW. 2008. Biogeographic and phylogenetic diversity of thermoacidophilic Cyanidiales in Yellowstone National Park, Japan, and New Zealand. Appl. Environ. Microbiol. 74:2822-2833.
Zeng X, Birrien JL, Fouquet Y, Cherkashov G, Jebbar M, Querellou J, et al. 2009. Pyrococcus CH1, an obligate piezophilic hyperthermophile: extending the upper pressuretemperature limits for life. ISME J. 3: 873-876.
Joseph B, Ramteke PW, Thomas G. 2008. Cold active microbial lipases: some hot issues and recent developments. Biotechnol. Adv. 26: 457-470.
Sarmiento F, Rocío P, Blamey JM. 2015. Cold and hot extremozymes: industrial relevance and current trends. Front. Bioeng. Biotechnol. 3: 1-15.
Schmid AK, Reiss DJ, Pan M, Koide T, Baliga NS. 2009. A single transcription factor regulates evolutionarily diverse but functionally linked metabolic pathways in response to nutrient availability. Mol. Syst. Biol. 5: 282-294.
Nicholas JR. 2006. Antarctic microorganism: coming in from the cold. Culture 27: 965-989.

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J. Microbiol. Biotechnol. 2017; 27(4): 649-659

Published online April 28, 2017 https://doi.org/10.4014/jmb.1611.11006

Extremozymes: A Potential Source for Industrial Applications

Kelly Dumorné ^1*, David Camacho Córdova ², Marcia Astorga-Eló ³ and Prabhaharan Renganathan ⁴

¹Departamento de Ingeniería Química, Facultad de Ciencias Químicas y Recursos Naturales, Universidad de La Frontera, Chile, ¹Department of Pharmaceutical Sciences, Faculty of Pharmaceutical Sciences of Ribeirao Preto, University of Sao Paulo-USP, Brazil, ²Department of Food Technology, University of Sonora, Mexico, ³Laboratorio Ecología Microbiana Aplicada, Departamento de Ingeniería Química, Facultad de Ciencias Químicas y Recursos Naturales,Universidad de La Frontera, Chile

Received: November 3, 2016; Accepted: January 19, 2017

Abstract

Extremophilic microorganisms have established a diversity of molecular strategies in order to
survive in extreme conditions. Biocatalysts isolated by these organisms are termed
extremozymes, and possess extraordinary properties of salt allowance, thermostability, and
cold adaptivity. Extremozymes are very resistant to extreme conditions owing to their great
solidity, and they pose new opportunities for biocatalysis and biotransformations, as well as
for the development of the economy and new line of research, through their application.
Thermophilic proteins, piezophilic proteins, acidophilic proteins, and halophilic proteins have
been studied during the last few years. Amylases, proteases, lipases, pullulanases, cellulases,
chitinases, xylanases, pectinases, isomerases, esterases, and dehydrogenases have great
potential application for biotechnology, such as in agricultural, chemical, biomedical, and
biotechnological processes. The study of extremozymes and their main applications have
emerged during recent years.

Keywords: Extremozymes, thermophiles, acidophiles, halophiles, biotechnology

Abstract

References

Cavicchioli R, Amils D, McGenity T. 2011. Life and applications of extremophiles. Environ. Microbiol. 13: 19031907.
Deppe U, Richnow HH, Michaelis W, Antranikian G. 2005. Degradation of crude oil by an arctic microbial consortium. Extremophiles 9: 461-470.
Navarro-González R, Iniguez E, de la Rosa J, McKay CR. 2009. Characterization of organics, microorganisms, desert soil, and Mars-like soils by thermal volatilization coupled to mass spectrometry and their implications for the search for organics on Mars by Phoenix and future space missions. Astrobiology 9: 703-711.
Seitz KH, Studdert C, Sanchez J, de Castro R. 1997. Intracellular proteolytic activity of the haloalkaliphilic archaeon Natronococcus occultus. Effect of starvation. J. Basic Microbiol. 7: 313-322.
Cárdenas JP, Valdés J, Quatrini R, Duarte F, Holmes DS. 2010. Lessons from the genomes of extremely acidophilic bacteria and archaea with special emphasis on bioleaching microorganisms. Appl. Microbiol. Biotechnol. 88: 605-620.
López-López O, Cerdán ME, González-Siso MI. 2014. New extremophilic lipases and esterases from metagenomics. Curr. Protein Pept. Sci. 15: 445-455.
Yildiz SY, Radchenkova N, Arga KY, Kambourova M, Toksoy OE. 2015. Genomic analysis of Brevibacillus thermoruber 423 reveals its biotechnological and industrial potential. Appl. Microbiol. Biotechnol. 99: 2277-2289.
Cowan DA, Ramond JB, Makhalanyane TP, De Maayer P. 2015. Metagenomics of extreme environments. Curr. Opin. Microbiol. 25: 97-102.
Qin J, Zhao B, Wang X. 2009. Non-sterilized fermentative production of polymer-grade L-lactic acid by a newly isolated thermophilic strain Bacillus sp. PLoS One 4: 43-59.
Karan R, Capes MD, DasSarma S. 2012. Function and biotechnology of extremophilic enzymes in low water activity. Aquat. Biosyst. 8: 3-15.
Nigam SP. 2013. Microbial enzymes with special characteristics for biotechnological applications. Biomolecules 3: 597-611.
Singh OV, Gabani P. 2011. Extremophiles: radiation resistance microbial reserves and therapeutic implications. J. Appl. Microbiol. 110: 851-861.
Demirjian DC, Morís-Varas F, Cassidy CS. 2001. Enzymes from extremophiles. Curr. Opin. Chem. Biol. 5: 144-151.
Van den Burg B. 2003. Extremophiles as a source for novel enzymes. Curr. Opin. Microbiol. 6: 213-218.
Irwin JA, Baird AW. 2004. Extremophiles and their application to veterinary medicine. Ir. Vet. J. 57: 348-354.
Díaz-Tenaa E, Rodríguez-Ezquerroa A, López de Lacalle Marcaide LN, Bustinduyb LG, Sáenzb AE. 2013. Use of extremophiles microorganisms for metal removal. Procedia Eng. 63: 67-74.
Eichler J. 2001. Biotechnological uses of archaeal extremozymes. Biotechnol. Adv. 19: 261-278.
Fujiwara S. 2002. Extremophiles: developments of their special functions and potential resources. J. Biosci. Bioeng. 94: 518-525.
Haki GD, Rakshit SK. 2003. Developments in industrially important thermostable enzymes: a review. Bioresour. Technol. 89: 7-34.
Raddadi N, Cherif A, Daffonchio D, Mohamed N, Fava F. 2015. Biotechnological applications of extremophiles, extremozymes and extremolytes. Appl. Microbiol. Biotechnol. 99: 7907-7913.
Dewan S. 2014. Global Markets for Enzymes in Industrial Applications. BCC Research, Wellesley, MA. USA.
Marhuenda-Egea FC, Piere-Velazquez S, Cadenas C, Cadenas E. 2002. An extreme halophilic enzyme active at low salt in reversed micelles. J. Biotechnol. 93: 159-164.
Jaenicke R, Schuring H, Beaucamp N, Ostendorp R. 1996. Structure and stability of hyperstable proteins: glycolytic enzymes from hyperthermophilic bacterium Thermotoga maritima. Adv. Protein Chem. 48: 181-269.
Sthal S. 1993. In Gupta MN (ed.). Thermostability of Enzymes, pp. 45-74. Springer, Berlin, Germany.
Cavicchioli R, Siddiqui KS, Andrews D, Sowers KR. 2002. Low-temperature extremophiles and their applications. Curr. Opin. Biotechnol. 13: 253-261.
Bertoldo C, Antranikian G. 2002. Starch-hydrolyzing enzymes from thermophilic archaea and bacteria. Curr. Opin. Chem. Biol. 6: 151-60.
Van der Maarel MJ, van der Veen B, Uitdehaag JC, Leemhuis H, Dijkhuizen L. 2002. Properties and application of starch-converting enzymes of the α-amylase family. J. Biotechnol. 94: 137-155.
Madigan MT, Marrs BL. 1997. Gli estremofili. Le Scienze 346: 78-85.
Sunna A, Bergquist PL. 2003. A gene encoding a novel extremely thermostable 1,4-beta-xylanase isolated directly from an environmental DNA sample. Extremophiles 7: 63-70.
Brasen C, Urbanke C, Schonheit P. 2005. A novel octameric AMP-forming acetyl-CoA synthetase from the hyperthermophilic crenarchaeon Pyrobaculum aerophilum. FEBS Lett. 579: 477482.
Mayer F, Küper U, Meyer C, Daxer S, Müller V, Rachel R, Huber H. 2012. AMP-forming acetyl coenzyme A synthetase in the outermost membrane of the hyperthermophilic crenarchaeon Ignicoccus hospitalis. J. Bacteriol. 194: 1572-1581.
Staiano M, Bazzicalupo P, Rossi M, D’Auria S. 2005. Glucose biosensors as models for the development of advanced protein-based biosensors. Mol. Biosyst. 1: 354-362.
Bruins ME, Janssen AE, Boom RM. 2001. Thermozymes and their applications: a review of recent literature and patents. Appl. Biochem. Biotechnol. 90: 155-186.
Jayakumar R, Jayashree S, Annapurna B, Seshadri S. 2012. Characterization of thermostable serine alkaline protease from an alkaliphilic strain Bacillus pumilus MCAS8 and its applications. Appl. Biochem. Biotechnol. 168: 1849-1866.
De Pascale D, Cusano AM, Author F, Parrilli E, di Prisco G, Marino G, Tutino ML. 2008. The cold-active Lip1 lipase from the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125 is a member of a new bacterial lipolytic enzyme family. Extremophiles 12: 311-323.
Unsworth LD, Van Der OJ, Koutsopoulos S. 2007. Hyperthermophilic enzymes - stability, activity and implementation strategies for high temperature applications. FEBS J. 274:4044-4056.
Rosenbaum E, Gabel F, Durá MA, Finet S, Cléry-Barraud C, Masson P, Franzetti B. 2012. Effects of hydrostatic pressure on the quaternary structure and enzymatic activity of a large peptidase complex from Pyrococcus horikoshii. Arch. Biochem. Biophys. 517: 104-110.
De Champdoré M, Staiano M, D’Auria S. 2007. Proteins from extremophiles as stable tools for advanced biotechnological applications of high social interest. J. R. Soc. Interface 4:183-191.
Boonyaratanakornkit BB, Park CB, Clark DS. 2002. Pressure effects on intra- and intermolecular interactions within proteins. Biochim. Biophys. Acta 1595: 235-249.
Fang J, Zhang L, Bazylinski DA. 2010. Deep-sea piezosphere and piezophiles: geomicrobiology and biogeochemistry. Trends Microbiol. 18: 413-422.
Reed CJ, Lewis H, Trejo E, Winston V, Evilia C. 2013. Protein adaptations in archaeal extremophiles. Archaea 2013: 373275.
Simonato F, Campanaro S, Lauro FM, Vezzi A, D’Angelo M, Vitulo N. 2006. Piezophilic adaptation: a genomic point of view. J. Biotechnol. 126: 11-25.
Takai K, Miyazaki M, Hirayama H, Nakagawa S, Querellou J, Godfroy A. 2009. Isolation and physiological characterization of two novel piezophilic, thermophilic chemolithoautotrophs from a deep-sea hydrothermal vent chimney. Environ. Micriobiol. 11: 1983-1997.
Fusi P, Grisa M, Mombelli E, Consonni R, Tortora P, Vanoni M. 1995. Expression of a synthetic gene encoding P2 ribonuclease from the extreme thermoacidophilic archaebacterium Sulfolobus solfataricus in mesophylic hosts. Gene 154: 99-103
Mombelli E, Shehi E, Fusi P, Tortora P. 2002. Exploring hyperthermophilic proteins under pressure: theoretical aspects and experimental findings. Biochim. Biophys. Acta 1595: 392-396.
Cavicchioli R. 2002. Extremophiles and the search for extraterrestrial life. Astrobiology 2: 281-292.
Georlette D, Blaise V, Collins T, D’Amico S, Gratia E, Hoyoux A, et al. 2004. Some like it cold: biocatalysis at low temperatures. FEMS Microbiol. Rev. 28: 25-42.
Gomes J, Steiner W. 1998. Production of a high activity of an extremely thermostable β-mannanase by the thermophilic eubacterium Rhodothermus marinus. Biotechnol. Lett. 20: 729733.
Gomes J, Gomes I, Terler K, Gubala N, Ditzelmuller G, Steiner W. 2000. Optimisation of culture medium and conditions for α-L-arabinofuranosidase production by the extreme thermophilic eubacterium Rhodothermus marinus. Enzyme Microb. Technol. 27: 414-422.
Abe F, Horikoshi K. 2001. The biotechnological potential of piezophiles. Trends Biotechnol. 19: 102-108.
Cannio R, Di Prizito N, Rossi M, Morana A. 2004. A xylandegrading strain of Sulfolobus solfataricus: isolation and characterization of the xylanase activity. Extremophiles 8:117-124.
Giuliano M, Schiraldi C, Marotta MR, Hugenholtz J, De Rosa M. 2004. Expression of Sulfolobus solfataricus αglucosidase in Lactococcus lactis. Appl. Microbiol. Biotechnol. 64: 829-832.
Jaenicke R. 1981. Enzymes under extreme of physical conditions. Annu. Rev. Biophys. Bioeng. 10: 1-67.
Huang Y, Krauss G, Cottaz H, Driguez H, Lipps G. 2005. A highly acid-stable and thermostable endo-β-glucanase from the thermoacidophilic archaeon Sulfolobus solfataricus. Biochem. J. 385: 581-588.
Golyshina O, Timmis KN. 2005. Ferroplasma and relatives, recently discovered cell wall-lacking archaea making a living in extremely acid, heavy metal-rich environments. Environ. Microbiol. 7: 1277-1288.
Sharma A, Kawarabayasi Y, Satyanarayana T. 2012. Acidophilic bacteria and archaea: acid stable biocatalysts and their potential applications. Extremophiles 16: 1-19.
Pikuta EV, Hoover RB, Tang J. 2007. Microbial extremophiles at the limits of life. Crit. Rev. Microbiol. 33: 183-209.
Hauenstein S, Zhang CM, Hou YM, Perona JJ. 2004. Shapeselective RNA recognition by cysteinyl-tRNA synthetase. Nat. Struct. Mol. Biol. 11: 1134-1141.
Szilágyi A, Závodszky P. 2000. Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Structure 8: 493-504.
Wright DB, Banks DD, Lohman JR, Hilsenbeck JL, Gloss LM. 2002. The effect of salts on the activity and stability of Escherichia coli and Haloferax volcanii dihydrofolate reductases. J. Mol. Biol. 323: 327-344.
Jackson BR, Noble C, Lavesa-Curto M, Bond PL, Bowater RP. 2007. Characterization of an ATP-dependent DNA ligase from the acidophilic archaeon “Ferroplasma acidarmanus” Fer1. Extremophiles 11: 315-327.
Delgado-García M, Valdivia-Urdiales B, Aguilar-González CN, Contreras-Esquivel JC, Rodríguez-Herrera R. 2012. Halophilic hydrolases as a new tool for the biotechnological industries. J. Sci. Food Agric. 92: 2575-2580.
Jackson CR, Langner HW, Donahoe-Christiansen J, Inskeep WP, McDermott TR. 2001. Molecular analysis of microbial community structure in an arsenite-oxidizing acidic thermal spring. Environ. Microbiol. 3: 532-542.
Datta S, Holmes B, Park J, Chen Z, Dibble DC, Hadi M, et al. 2010. Ionic liquid tolerant hyperthermophilic cellulases for biomass pretreatment and hydrolysis. Green Chem. 12: 338345.
Madern D, Pfister C, Zaccai G. 1995. Mutation at a single acidic amino acid enhances the halophilic behaviour of malate dehydrogenase from Haloarcula marismortui in physiological salts. Eur. J. Biochem. 3: 1088-1095.
Raddadi N, Cherif A, Daffonchio D, Fava F. 2013. Haloalkalitolerant and thermostable cellulases with improved tolerance to ionic liquids and organic solvents from Paenibacillus tarimensis isolated from the Chott El Fejej, Sahara desert, Tunisia. Bioresour. Technol. 150: 121-128.
Bhalla A, Bansal N, Kumar S, Bischoff KM, Sani RK. 2013. Improved lignocellulose conversion to biofuels with thermophilic bacteria and thermostable enzymes. Bioresour. Technol. 128: 751-759.
Elleuche S, Schröder C, Sahm K, Antranikian G. 2014. Extremozymes - biocatalysts with unique properties from extremophilic microorganisms. Curr. Opin. Biotechnol. 29:116-123.
Madern D, Ebel C, Zaccai G. 2000. Halophilic adaptation of enzymes. Extremophiles 4: 91-98.
Sutrisno A, Ueda M, Abe Y, Nakazawa M, Miyatake K. 2004. A chitinase with high activity toward partially Nacetylated chitosan from a new, moderately thermophilic, chitin-degrading bacterium, Ralstonia sp. A-471. Appl. Microbiol. Biotechnol. 63: 398-406.
Taylor INR, Brown C, Rycroft M, King G, Littlechild JA, Lloyd MC, et al. 2004. Application of thermophilic enzymes in commercial biotransformation processes. Biochem. Soc. Trans. 32: 290-292.
Woosowska S, Synowiecki J. 2004. Thermostable glucosidase with broad substrate specificity suitable for processing of lactose-containing products. Food Chem. 85: 181-187.
Litchfield CD. 2011. Potential for industrial products from the halophilic Archaea. J. Ind. Microbiol. Biotechnol. 38:1635-1647.
Schreck SD, Grunden AM. 2014. Biotechnological applications of halophilic lipases and thioesterases. Appl. Microbiol. Biotechnol. 98: 1011-1021.
Ortega G, Laín A, Tadeo X, López-Méndez B, Castaño D, Milleta O. 2011. Halophilic enzyme activation induced by salts. Sci. Rep. 1: 6.
Serour E, Antranikian G. 2002. Novel thermoactive glucoamylases from the thermoacidophilic Archaea Thermoplasma acidophilum, Picrophilus torridus and Picrophilus oshimae. Antonie Van Leeuwenhoek 81: 73-83.
Suzuki T, Nakayama T, Kurihara T, Nishino T, Esaki N. 2001. Cold-active lipolytic activity of psychrotrophic Acinetobacter sp. strain no. 6. J. Biosci. Bioeng. 92: 144-148.
Kim J, Dordick S. 1997. Unusual salt and solvent dependence of a protease from an extreme halophile. Biotechnol. Bioeng. 55: 471-479.
Karbalaei-Heidari HR, Ziaee AA, Amoozegar MA. 2007. Purification and biochemical characterization of a protease secreted by the Salinivibrio sp. strain AF-2004 and its behavior in organic solvents. Extremophiles 11: 237-243.
Ruiz DM, De Castro RE. 2007. Effect of organic solvents on the activity and stability of an extracellular protease secreted by the haloalkaliphilic archaeon Natrialba magadii. J. Ind. Microbiol. Biotechnol. 34: 111-115.
Fukushima T, Mizuki T, Echigo A, Inoue A, Usami R. 2005. Organic solvent tolerance of halophilic a-amylase from a haloarchaeon, Haloarcula sp. strain S-1. Extremophiles 9: 85-89.
Shafiei M, Ziaee AA, Amoozegar MA. 2011. Purification and characterization of an organic-solvent-tolerant halophilic a-amylase from the moderately halophilic Nesterenkonia sp. strain F. J. Ind. Microbiol. Biotechnol. 38: 275-281.
Yu HY, Li X. 2012. Purification and characterization of novel organic-solvent-tolerant b-amylase and serine protease from a newly isolated Salimicrobium halophilum strain LY20. FEMS Microbiol. Lett 329: 204-211.
Munawar N, Engel PC. 2012. Overexpression in a non-native halophilic host and biotechnological potential of NAD+dependent glutamate dehydrogenase from Halobacterium salinarum strain NRC-36014. Extremophiles 16: 463-476.
Vidyasagar M, Prakash S, Sreeramulu K. 2006. Optimization of culture conditions for the production of haloalkaliphilic thermostable protease from an extremely halophilic archaeon Halogeometricum borinquense sp. TSS 101. Lett. Appl. Microbiol. 43: 385-391.
Zaccai G. 2004. The effect of water on protein dynamics. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359: 1269-1275.
Sellek GA, Chaudhuri JB. 1999. Biocatalysis in organic media using enzymes from extremophiles. Enzyme Microb. Technol. l25: 471-482.
Cordone L, Ferrand M, Vitrano E, Zaccai G. 1999. Harmonic behavior of trehalose-coated carbon-monoxymyoglobin at high temperature. Biophys. J. 76: 1043-1047.
Lehnert U, Réat V, Weik M, Zaccaï G, Pfister C. 1998. Thermal motions in bacteriorhodopsin at different hydration levels studied by neutron scattering: correlation with kinetics and light-induced conformational changes. Biophys. J. 75:1945-1952.
Singh A, Kuhad RC, Ward OP. 2007. Industrial application of microbial cellulases, pp. 345-358. In Kuhad RC, Singh A (eds.). Lignocellulose Biotechnology: Future Prospects. I.K. International Publishing House, New Delhi, India.
Merlino A, Russo KI, Castellano I, De VE, Rossi B, Conte M, et al. 2010. Structure and flexibility in cold-adapted iron superoxide dismutases: the case of the enzyme isolated from Pseudoalteromonas haloplanktis. J. Struct. Biol. 172: 343352.
Siddiqui KS, Cavicchioli R. 2006. Cold-adapted enzymes. Annu. Rev. Biochem. 75: 403-433.
Sukumaran RK, Singhania RR, Pandey A. 2005. Microbial cellulases - production, applications and challenges. J. Sci. Ind. Res. 64: 832-844.
Kumar L, Awasthi G, Singh B. 2011. Extremophiles: a novel source of industrially important enzymes. Biotechnol. Appl. Biochem. 10: 1-15.
Gerday C, Aittaleb M, Bentahir M, Chessa JP, Claverie P, Collins T, et al. 2000. Cold-adapted enzymes: from fundamentals to biotechnology. Trends Biotechnol. 18: 103-107.
Huston AL. 2008. Biotechnological aspects of cold-adapted enzymes, pp. 347-363. In Margesin R, Schinner F, Marx J-C, Gerday C (eds.). Psychrophiles: From Biodiversity to Biotechnology. Springer, Heidelberg. Germany.
Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S, et al. 2012. A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS One 7: e48479.
Rolli E, Marasco M, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, et al. 2015. Improved plant resistance to drought is promoted by the root-associated microbiome as water stress-dependent trait. Environ. Microbiol. 17: 316-331.
Hotta Y, Ezaki S, Atomi H, Imanaka T. 2002. Extremely stable and versatile carboxylesterase from a hyperthermophilic archaeon. Appl. Environ. Microbiol. 68: 3925-3931.
Johnson DB. 2014. Biomining - biotechnologies for extracting and recovering metals from ores and waste materials. Curr. Opin. Biotechnol. 30: 24-31.
Karasová-Lipovová P, Strnad H, Spiwok V, Malá S, Králová B, Russell NJ. 2003. The cloning, purification and characterisation of a cold-active β-galactosidase from the psychrotolerant Antarctic bacterium Arthrobacter sp. C2-2. Enzyme Microb. Technol. 33: 836-844.
Navarro CA, von Bernath D, Jerez CA. 2013. Heavy metal resistance strategies of acidophilic bacteria and their acquisition: importance for biomining and bioremediation. Biol. Res. 46: 363-371.
Adrio JL, Demain AL. 2014. Microbial enzymes: tools for biotechnological processes. Biomolecules 4: 117-139.
Karmakar M, Ray RR. 2011. Current trends in research and application of microbial cellulases. Res. J. Microbiol. 6: 4153.
Birgisson H, Delgado O, Arroyo LG, Hatti-Kaul R, Mattiasson B. 2003. Cold-adapted yeasts as producers of cold-active polygalacturonases. Extremophiles 7: 185-193.
Singh BK. 2010. Exploring microbial diversity for biotechnology:the way forward. Trends Biotechnol. 28: 111-116.
Hess M, Katzer M, Antranikian G. 2008. Extremely thermostable esterases from the thermoacidophilic euryarchaeon Picrophilus torridus. Extremophiles 12: 351-364.
Staley JT, Konopka A. 1985. Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu. Rev. Microbiol. 39: 321-346.
Young P. 1997. Major microbial diversity initiative recommended. ASM News 63: 417-421.
Mohammed K, Pramod WR. 2009. Cold-active extracellular alkaline protease from an alkaliphilic Stenotrophomonas maltophilia: production of enzyme and its industrial applications. Can. J. Microbiol. 55: 1294-1301.
Yumoto I. 2002. Bioenergetics of alkaliphilic Bacillus spp. J. Biosci. Bioeng. 93: 342-353.
Chang P, Tsai WS, Tsai CL, Tseng MJ. 2004. Cloning and characterization of two thermostable xylanases from an alkaliphilic Bacillus firmus. Biochem. Biophys. Res. Commun. 319: 1017-1025.
Das H, Sing SK. 2004. Useful byproducts from cellulosic waste of agriculture and food industry - a critical appraisal. Crit. Rev. Food Sci. Nutr. 44: 77-89.
Hashim SO, Delgado O, Hatti-Kaul R, Mulaa FJ, Mattiasson B. 2004. Starch hydrolysing Bacillus halodurans isolates from a Kenyan soda lake. Biotechnol. Lett. 26: 823-828.
Von Solingen P, Meijer D, Kleij WA, Branett C, Bolle R, Power SD, Jones BE. 2001. Cloning and expression of an endocellulase gene from a novel streptomycete isolated from an East African soda lake. Extremophiles 5: 333-341.
Ma Y, Xue Y, Grant WD, Collins NC, Duckworth AW, Van Steenbergen RP, Jones BE. 2004. Alkalimonas amylolytica gen. nov., sp. nov., and Alkalimonas delamerensis gen. nov., sp. nov., novel alkaliphilic bacteria from soda lakes in China and East Africa. Extremophiles 8: 193-200.
Margesin R, Schinner F, Marx JC, Gerday C (eds.). 2008. Psychrophiles: From Biodiversity to Biotechnology. SpringerVerlag, Berlin-Heidelberg. Germany.
Zeng R, Zhang R, Zhao J, Lin N. 2003. Cold-active serine alkaline protease from the psychrophilic bacterium Pseudomonas strain DY-A: enzyme purification and characterization. Extremophiles 7: 335-337.
Collins T, D’Amico S, Marx JC, Feller G, Gerday C. 2007. Cold-adapted enzymes, pp. 165-179. In Gerday C, Glansdorff N (eds.). Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. USA.
Gurung N, Ray S, Bose S, Rai V. 2013. A broader view:microbial enzymes and their relevance in industries, medicine, and beyond. Biomed. Res. Int. 2013: 329121.
Egorova K, Antranikian G. 2005. Industrial relevance of thermophilic Archaea. Curr. Opin. Microbiol. 8: 649-655.
Ferrer M, Golyshina O, Beloqui A, Golyshin PN. 2007. Mining enzymes from extreme environments. Curr. Opin. Microbiol. 10: 207-214.
Secades P, Alvarez B, Guijarro JA. 2003. Purification and properties of a new psychrophilic metalloprotease (Fpp2) in the fish pathogen Flavobacterium psychrophilum. FEMS Microbiol. Lett. 226: 273-279.
Huang H, Luo H, Wang Y, Fu D, Shao N, Yang P, et al. 2009. Novel low-temperature-active phytase from Erwinia carotovora var. carotovota ACCC 10276. J. Microbiol. Biotechnol. 19: 1085-1091.
Tutino ML, di Prisco G, Marino G, de Pascale D. 2009. Cold-adapted esterases and lipases: from fundamentals to application. Protein Pept. Lett. 16: 1172-1180.
Ueda M, Goto T, Nakazawa M, Miyatake K, Sakaguchi M, Inouye K. 2010. A novel cold-adapted cellulase complex from Eisenia foetida: characterization of a multienzyme complex with carboxymethylcellulase, beta-glucosidase, beta-1,3 glucanase, and beta-xylosidase. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 157: 26-32.
Wang F, Hao J, Yang C, Sun M. 2010. Cloning, expression, and identification of a novel extracellular cold-adapted alkaline protease gene of the marine bacterium strain YS80-122. Appl. Biochem. Biotechnol. 162: 1497-1505.
Parkes R, Cragg J, Banning BA, Brock N, Webster F, Fry G, et al. 2007. Biogeochemistry and biodiversity of methane cycling in subsurface marine sediments (Skagerrak, Denmark). Environ. Microbiol. 9: 1146-1161.
Aurilia V, Parracino A, D’Auria S. 2008. Microbial carbohydrate esterases in cold adapted environments. Gene 410: 234-240.
Toplin JA, Norris TB, Lehr CR, McDermott TR, Castenholz RW. 2008. Biogeographic and phylogenetic diversity of thermoacidophilic Cyanidiales in Yellowstone National Park, Japan, and New Zealand. Appl. Environ. Microbiol. 74:2822-2833.
Zeng X, Birrien JL, Fouquet Y, Cherkashov G, Jebbar M, Querellou J, et al. 2009. Pyrococcus CH1, an obligate piezophilic hyperthermophile: extending the upper pressuretemperature limits for life. ISME J. 3: 873-876.
Joseph B, Ramteke PW, Thomas G. 2008. Cold active microbial lipases: some hot issues and recent developments. Biotechnol. Adv. 26: 457-470.
Sarmiento F, Rocío P, Blamey JM. 2015. Cold and hot extremozymes: industrial relevance and current trends. Front. Bioeng. Biotechnol. 3: 1-15.
Schmid AK, Reiss DJ, Pan M, Koide T, Baliga NS. 2009. A single transcription factor regulates evolutionarily diverse but functionally linked metabolic pathways in response to nutrient availability. Mol. Syst. Biol. 5: 282-294.
Nicholas JR. 2006. Antarctic microorganism: coming in from the cold. Culture 27: 965-989.