DOI QR코드

DOI QR Code

Extremozymes: A Potential Source for Industrial Applications

  • Dumorne, Kelly (Departamento de Ingenieria Quimica, Facultad de Ciencias Quimicas y Recursos Naturales, Universidad de La Frontera) ;
  • Cordova, David Camacho (Department of Pharmaceutical Sciences, Faculty of Pharmaceutical Sciences of Ribeirao Preto, University of Sao Paulo-USP) ;
  • Astorga-Elo, Marcia (Department of Food Technology, University of Sonora) ;
  • Renganathan, Prabhaharan (Laboratorio Ecologia Microbiana Aplicada, Departamento de Ingenieria Quimica, Facultad de Ciencias Quimicas y Recursos Naturales, Universidad de La Frontera)
  • Received : 2016.11.03
  • Accepted : 2017.01.19
  • Published : 2017.04.28

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

References

  1. Cavicchioli R, Amils D, McGenity T. 2011. Life and applications of extremophiles. Environ. Microbiol. 13: 1903-1907. https://doi.org/10.1111/j.1462-2920.2011.02512.x
  2. Deppe U, Richnow HH, Michaelis W, Antranikian G. 2005. Degradation of crude oil by an arctic microbial consortium. Extremophiles 9: 461-470. https://doi.org/10.1007/s00792-005-0463-2
  3. Navarro-Gonzalez 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. https://doi.org/10.1089/ast.2008.0284
  4. 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.
  5. Cardenas JP, Valdes 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. https://doi.org/10.1007/s00253-010-2795-9
  6. Lopez-Lopez O, Cerdan ME, Gonzalez-Siso MI. 2014. New extremophilic lipases and esterases from metagenomics. Curr. Protein Pept. Sci. 15: 445-455. https://doi.org/10.2174/1389203715666140228153801
  7. 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. https://doi.org/10.1007/s00253-015-6388-5
  8. Cowan DA, Ramond JB, Makhalanyane TP, De Maayer P. 2015. Metagenomics of extreme environments. Curr. Opin. Microbiol. 25: 97-102. https://doi.org/10.1016/j.mib.2015.05.005
  9. 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.
  10. Karan R, Capes MD, DasSarma S. 2012. Function and biotechnology of extremophilic enzymes in low water activity. Aquat. Biosyst. 8: 3-15. https://doi.org/10.1186/2046-9063-8-3
  11. Nigam SP. 2013. Microbial enzymes with special characteristics for biotechnological applications. Biomolecules 3: 597-611. https://doi.org/10.3390/biom3030597
  12. Singh OV, Gabani P. 2011. Extremophiles: radiation resistance microbial reserves and therapeutic implications. J. Appl. Microbiol. 110: 851-861. https://doi.org/10.1111/j.1365-2672.2011.04971.x
  13. Demirjian DC, Morís-Varas F, Cassidy CS. 2001. Enzymes from extremophiles. Curr. Opin. Chem. Biol. 5: 144-151. https://doi.org/10.1016/S1367-5931(00)00183-6
  14. Van den Burg B. 2003. Extremophiles as a source for novel enzymes. Curr. Opin. Microbiol. 6: 213-218. https://doi.org/10.1016/S1369-5274(03)00060-2
  15. Irwin JA, Baird AW. 2004. Extremophiles and their application to veterinary medicine. Ir. Vet. J. 57: 348-354. https://doi.org/10.1186/2046-0481-57-6-348
  16. Diaz-Tenaa E, Rodriguez-Ezquerroa A, Lopez de Lacalle Marcaide LN, Bustinduyb LG, Saenzb AE. 2013. Use of extremophiles microorganisms for metal removal. Procedia Eng. 63: 67-74. https://doi.org/10.1016/j.proeng.2013.08.197
  17. Eichler J. 2001. Biotechnological uses of archaeal extremozymes. Biotechnol. Adv. 19: 261-278. https://doi.org/10.1016/S0734-9750(01)00061-1
  18. Fujiwara S. 2002. Extremophiles: developments of their special functions and potential resources. J. Biosci. Bioeng. 94: 518-525. https://doi.org/10.1016/S1389-1723(02)80189-X
  19. Haki GD, Rakshit SK. 2003. Developments in industrially important thermostable enzymes: a review. Bioresour. Technol. 89: 7-34.
  20. Raddadi N, Cherif A, Daffonchio D, Mohamed N, Fava F. 2015. Biotechnological applications of extremophiles, extremozymes and extremolytes. Appl. Microbiol. Biotechnol. 99: 7907-7913. https://doi.org/10.1007/s00253-015-6874-9
  21. Dewan S. 2014. Global Markets for Enzymes in Industrial Applications. BCC Research, Wellesley, MA. USA.
  22. 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. https://doi.org/10.1016/S0168-1656(01)00392-3
  23. 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.
  24. Sthal S. 1993. In Gupta MN (ed.). Thermostability of Enzymes, pp. 45-74. Springer, Berlin, Germany.
  25. Cavicchioli R, Siddiqui KS, Andrews D, Sowers KR. 2002. Low-temperature extremophiles and their applications. Curr. Opin. Biotechnol. 13: 253-261. https://doi.org/10.1016/S0958-1669(02)00317-8
  26. Bertoldo C, Antranikian G. 2002. Starch-hydrolyzing enzymes from thermophilic archaea and bacteria. Curr. Opin. Chem. Biol. 6: 151-60. https://doi.org/10.1016/S1367-5931(02)00311-3
  27. Van der Maarel MJ, van der Veen B, Uitdehaag JC, Leemhuis H, Dijkhuizen L. 2002. Properties and application of starch-converting enzymes of the $\alpha$-amylase family. J. Biotechnol. 94: 137-155. https://doi.org/10.1016/S0168-1656(01)00407-2
  28. Madigan MT, Marrs BL. 1997. Gli estremofili. Le Scienze 346: 78-85.
  29. 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.
  30. Brasen C, Urbanke C, Schonheit P. 2005. A novel octameric AMP-forming acetyl-CoA synthetase from the hyperthermophilic crenarchaeon Pyrobaculum aerophilum. FEBS Lett. 579: 477-482. https://doi.org/10.1016/j.febslet.2004.12.016
  31. Mayer F, Kuper U, Meyer C, Daxer S, Muller 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. https://doi.org/10.1128/JB.06130-11
  32. 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. https://doi.org/10.1039/b513385h
  33. Bruins ME, Janssen AE, Boom RM. 2001. Thermozymes and their applications: a review of recent literature and patents. Appl. Biochem. Biotechnol. 90: 155-186. https://doi.org/10.1385/ABAB:90:2:155
  34. 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. https://doi.org/10.1007/s12010-012-9902-6
  35. 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. https://doi.org/10.1007/s00792-008-0163-9
  36. Unsworth LD, Van Der OJ, Koutsopoulos S. 2007. Hyperthermophilic enzymes - stability, activity and implementation strategies for high temperature applications. FEBS J. 274: 4044-4056. https://doi.org/10.1111/j.1742-4658.2007.05954.x
  37. Rosenbaum E, Gabel F, Dura MA, Finet S, Clery-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. https://doi.org/10.1016/j.abb.2011.07.017
  38. De Champdore 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. https://doi.org/10.1098/rsif.2006.0174
  39. Boonyaratanakornkit BB, Park CB, Clark DS. 2002. Pressure effects on intra- and intermolecular interactions within proteins. Biochim. Biophys. Acta 1595: 235-249. https://doi.org/10.1016/S0167-4838(01)00347-8
  40. Fang J, Zhang L, Bazylinski DA. 2010. Deep-sea piezosphere and piezophiles: geomicrobiology and biogeochemistry. Trends Microbiol. 18: 413-422. https://doi.org/10.1016/j.tim.2010.06.006
  41. Reed CJ, Lewis H, Trejo E, Winston V, Evilia C. 2013. Protein adaptations in archaeal extremophiles. Archaea 2013: 373275.
  42. 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. https://doi.org/10.1016/j.jbiotec.2006.03.038
  43. 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. https://doi.org/10.1111/j.1462-2920.2009.01921.x
  44. 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 https://doi.org/10.1016/0378-1119(94)00828-G
  45. 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. https://doi.org/10.1016/S0167-4838(01)00361-2
  46. Cavicchioli R. 2002. Extremophiles and the search for extraterrestrial life. Astrobiology 2: 281-292. https://doi.org/10.1089/153110702762027862
  47. 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. https://doi.org/10.1016/j.femsre.2003.07.003
  48. Gomes J, Steiner W. 1998. Production of a high activity of an extremely thermostable $\beta$-mannanase by the thermophilic eubacterium Rhodothermus marinus. Biotechnol. Lett. 20: 729-733. https://doi.org/10.1023/A:1005330618613
  49. Gomes J, Gomes I, Terler K, Gubala N, Ditzelmuller G, Steiner W. 2000. Optimisation of culture medium and conditions for $\alpha$-L-arabinofuranosidase production by the extreme thermophilic eubacterium Rhodothermus marinus. Enzyme Microb. Technol. 27: 414-422. https://doi.org/10.1016/S0141-0229(00)00229-5
  50. Abe F, Horikoshi K. 2001. The biotechnological potential of piezophiles. Trends Biotechnol. 19: 102-108. https://doi.org/10.1016/S0167-7799(00)01539-0
  51. Cannio R, Di Prizito N, Rossi M, Morana A. 2004. A xylan-degrading strain of Sulfolobus solfataricus: isolation and characterization of the xylanase activity. Extremophiles 8: 117-124. https://doi.org/10.1007/s00792-003-0370-3
  52. Giuliano M, Schiraldi C, Marotta MR, Hugenholtz J, De Rosa M. 2004. Expression of Sulfolobus solfataricus $\alpha$-glucosidase in Lactococcus lactis. Appl. Microbiol. Biotechnol. 64: 829-832. https://doi.org/10.1007/s00253-003-1493-2
  53. Jaenicke R. 1981. Enzymes under extreme of physical conditions. Annu. Rev. Biophys. Bioeng. 10: 1-67. https://doi.org/10.1146/annurev.bb.10.060181.000245
  54. Huang Y, Krauss G, Cottaz H, Driguez H, Lipps G. 2005. A highly acid-stable and thermostable endo-$\beta$-glucanase from the thermoacidophilic archaeon Sulfolobus solfataricus. Biochem. J. 385: 581-588. https://doi.org/10.1042/BJ20041388
  55. 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. https://doi.org/10.1111/j.1462-2920.2005.00861.x
  56. Sharma A, Kawarabayasi Y, Satyanarayana T. 2012. Acidophilic bacteria and archaea: acid stable biocatalysts and their potential applications. Extremophiles 16: 1-19. https://doi.org/10.1007/s00792-011-0402-3
  57. Pikuta EV, Hoover RB, Tang J. 2007. Microbial extremophiles at the limits of life. Crit. Rev. Microbiol. 33: 183-209. https://doi.org/10.1080/10408410701451948
  58. Hauenstein S, Zhang CM, Hou YM, Perona JJ. 2004. Shape-selective RNA recognition by cysteinyl-tRNA synthetase. Nat. Struct. Mol. Biol. 11: 1134-1141. https://doi.org/10.1038/nsmb849
  59. Szilagyi A, Zavodszky P. 2000. Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Structure 8: 493-504. https://doi.org/10.1016/S0969-2126(00)00133-7
  60. 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. https://doi.org/10.1016/S0022-2836(02)00916-6
  61. 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. https://doi.org/10.1007/s00792-006-0041-2
  62. Delgado-Garcia M, Valdivia-Urdiales B, Aguilar-Gonzalez CN, Contreras-Esquivel JC, Rodriguez-Herrera R. 2012. Halophilic hydrolases as a new tool for the biotechnological industries. J. Sci. Food Agric. 92: 2575-2580. https://doi.org/10.1002/jsfa.5860
  63. 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. https://doi.org/10.1046/j.1462-2920.2001.00221.x
  64. 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: 338-345. https://doi.org/10.1039/b916564a
  65. 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.
  66. Raddadi N, Cherif A, Daffonchio D, Fava F. 2013. Halo-alkalitolerant 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. https://doi.org/10.1016/j.biortech.2013.09.089
  67. 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. https://doi.org/10.1016/j.biortech.2012.10.145
  68. Elleuche S, Schroder C, Sahm K, Antranikian G. 2014. Extremozymes - biocatalysts with unique properties from extremophilic microorganisms. Curr. Opin. Biotechnol. 29: 116-123.
  69. Madern D, Ebel C, Zaccai G. 2000. Halophilic adaptation of enzymes. Extremophiles 4: 91-98. https://doi.org/10.1007/s007920050142
  70. Sutrisno A, Ueda M, Abe Y, Nakazawa M, Miyatake K. 2004. A chitinase with high activity toward partially N-acetylated chitosan from a new, moderately thermophilic, chitin-degrading bacterium, Ralstonia sp. A-471. Appl. Microbiol. Biotechnol. 63: 398-406. https://doi.org/10.1007/s00253-003-1351-2
  71. 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. https://doi.org/10.1042/bst0320290
  72. Woosowska S, Synowiecki J. 2004. Thermostable glucosidase with broad substrate specificity suitable for processing of lactose-containing products. Food Chem. 85: 181-187. https://doi.org/10.1016/S0308-8146(03)00104-3
  73. Litchfield CD. 2011. Potential for industrial products from the halophilic Archaea. J. Ind. Microbiol. Biotechnol. 38: 1635-1647. https://doi.org/10.1007/s10295-011-1021-9
  74. Schreck SD, Grunden AM. 2014. Biotechnological applications of halophilic lipases and thioesterases. Appl. Microbiol. Biotechnol. 98: 1011-1021. https://doi.org/10.1007/s00253-013-5417-5
  75. Ortega G, Lain A, Tadeo X, Lopez-Mendez B, Castano D, Milleta O. 2011. Halophilic enzyme activation induced by salts. Sci. Rep. 1: 6. https://doi.org/10.1038/srep00006
  76. 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. https://doi.org/10.1023/A:1020525525490
  77. 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. https://doi.org/10.1016/S1389-1723(01)80215-2
  78. Kim J, Dordick S. 1997. Unusual salt and solvent dependence of a protease from an extreme halophile. Biotechnol. Bioeng. 55: 471-479. https://doi.org/10.1002/(SICI)1097-0290(19970805)55:3<471::AID-BIT2>3.0.CO;2-9
  79. 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. https://doi.org/10.1007/s00792-006-0031-4
  80. 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. https://doi.org/10.1007/s10295-006-0174-4
  81. 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. https://doi.org/10.1007/s00792-004-0423-2
  82. 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. https://doi.org/10.1007/s10295-010-0770-1
  83. 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. https://doi.org/10.1111/j.1574-6968.2012.02522.x
  84. 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. https://doi.org/10.1007/s00792-012-0446-z
  85. 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. https://doi.org/10.1111/j.1472-765X.2006.01980.x
  86. Zaccai G. 2004. The effect of water on protein dynamics. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359: 1269-1275. https://doi.org/10.1098/rstb.2004.1503
  87. Sellek GA, Chaudhuri JB. 1999. Biocatalysis in organic media using enzymes from extremophiles. Enzyme Microb. Technol. l25: 471-482.
  88. Cordone L, Ferrand M, Vitrano E, Zaccai G. 1999. Harmonic behavior of trehalose-coated carbon-monoxy-myoglobin at high temperature. Biophys. J. 76: 1043-1047. https://doi.org/10.1016/S0006-3495(99)77269-3
  89. Lehnert U, Reat V, Weik M, Zaccai 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. https://doi.org/10.1016/S0006-3495(98)77635-0
  90. 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.
  91. 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: 343-352. https://doi.org/10.1016/j.jsb.2010.08.008
  92. Siddiqui KS, Cavicchioli R. 2006. Cold-adapted enzymes. Annu. Rev. Biochem. 75: 403-433. https://doi.org/10.1146/annurev.biochem.75.103004.142723
  93. Sukumaran RK, Singhania RR, Pandey A. 2005. Microbial cellulases - production, applications and challenges. J. Sci. Ind. Res. 64: 832-844.
  94. Kumar L, Awasthi G, Singh B. 2011. Extremophiles: a novel source of industrially important enzymes. Biotechnol. Appl. Biochem. 10: 1-15.
  95. 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. https://doi.org/10.1016/S0167-7799(99)01413-4
  96. 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.
  97. 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. https://doi.org/10.1371/journal.pone.0048479
  98. 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. https://doi.org/10.1111/1462-2920.12439
  99. Hotta Y, Ezaki S, Atomi H, Imanaka T. 2002. Extremely stable and versatile carboxylesterase from a hyperthermophilic archaeon. Appl. Environ. Microbiol. 68: 3925-3931. https://doi.org/10.1128/AEM.68.8.3925-3931.2002
  100. Johnson DB. 2014. Biomining - biotechnologies for extracting and recovering metals from ores and waste materials. Curr. Opin. Biotechnol. 30: 24-31. https://doi.org/10.1016/j.copbio.2014.04.008
  101. Karasova-Lipovova P, Strnad H, Spiwok V, Mala S, Kralova B, Russell NJ. 2003. The cloning, purification and characterisation of a cold-active $\beta$-galactosidase from the psychrotolerant Antarctic bacterium Arthrobacter sp. C2-2. Enzyme Microb. Technol. 33: 836-844. https://doi.org/10.1016/S0141-0229(03)00211-4
  102. 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. https://doi.org/10.4067/S0716-97602013000400008
  103. Adrio JL, Demain AL. 2014. Microbial enzymes: tools for biotechnological processes. Biomolecules 4: 117-139. https://doi.org/10.3390/biom4010117
  104. Karmakar M, Ray RR. 2011. Current trends in research and application of microbial cellulases. Res. J. Microbiol. 6: 41-53. https://doi.org/10.3923/jm.2011.41.53
  105. 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.
  106. Singh BK. 2010. Exploring microbial diversity for biotechnology: the way forward. Trends Biotechnol. 28: 111-116. https://doi.org/10.1016/j.tibtech.2009.11.006
  107. Hess M, Katzer M, Antranikian G. 2008. Extremely thermostable esterases from the thermoacidophilic euryarchaeon Picrophilus torridus. Extremophiles 12: 351-364. https://doi.org/10.1007/s00792-008-0139-9
  108. Staley JT, Konopka A. 1985. Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu. Rev. Microbiol. 39: 321-346. https://doi.org/10.1146/annurev.mi.39.100185.001541
  109. Young P. 1997. Major microbial diversity initiative recommended. ASM News 63: 417-421.
  110. 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. https://doi.org/10.1139/W09-089
  111. Yumoto I. 2002. Bioenergetics of alkaliphilic Bacillus spp. J. Biosci. Bioeng. 93: 342-353. https://doi.org/10.1016/S1389-1723(02)80066-4
  112. 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. https://doi.org/10.1016/j.bbrc.2004.05.078
  113. 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. https://doi.org/10.1080/10408690490424630
  114. 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. https://doi.org/10.1023/B:BILE.0000025885.19910.d7
  115. 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. https://doi.org/10.1007/s007920100198
  116. 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. https://doi.org/10.1007/s00792-004-0377-4
  117. Margesin R, Schinner F, Marx JC, Gerday C (eds.). 2008. Psychrophiles: From Biodiversity to Biotechnology. Springer-Verlag, Berlin-Heidelberg. Germany.
  118. 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. https://doi.org/10.1007/s00792-003-0323-x
  119. 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.
  120. 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.
  121. Egorova K, Antranikian G. 2005. Industrial relevance of thermophilic Archaea. Curr. Opin. Microbiol. 8: 649-655. https://doi.org/10.1016/j.mib.2005.10.015
  122. Ferrer M, Golyshina O, Beloqui A, Golyshin PN. 2007. Mining enzymes from extreme environments. Curr. Opin. Microbiol. 10: 207-214. https://doi.org/10.1016/j.mib.2007.05.004
  123. 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. https://doi.org/10.1016/S0378-1097(03)00599-8
  124. 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.
  125. 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. https://doi.org/10.2174/092986609789071270
  126. 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. https://doi.org/10.1016/j.cbpb.2010.04.014
  127. 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 YS-80-122. Appl. Biochem. Biotechnol. 162: 1497-1505. https://doi.org/10.1007/s12010-010-8927-y
  128. 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. https://doi.org/10.1111/j.1462-2920.2006.01237.x
  129. Aurilia V, Parracino A, D'Auria S. 2008. Microbial carbohydrate esterases in cold adapted environments. Gene 410: 234-240. https://doi.org/10.1016/j.gene.2007.12.019
  130. 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. https://doi.org/10.1128/AEM.02741-07
  131. Zeng X, Birrien JL, Fouquet Y, Cherkashov G, Jebbar M, Querellou J, et al. 2009. Pyrococcus CH1, an obligate piezophilic hyperthermophile: extending the upper pressure-temperature limits for life. ISME J. 3: 873-876. https://doi.org/10.1038/ismej.2009.21
  132. Joseph B, Ramteke PW, Thomas G. 2008. Cold active microbial lipases: some hot issues and recent developments. Biotechnol. Adv. 26: 457-470. https://doi.org/10.1016/j.biotechadv.2008.05.003
  133. Sarmiento F, Rocio P, Blamey JM. 2015. Cold and hot extremozymes: industrial relevance and current trends. Front. Bioeng. Biotechnol. 3: 1-15.
  134. 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.
  135. Nicholas JR. 2006. Antarctic microorganism: coming in from the cold. Culture 27: 965-989.

Cited by

  1. Purine and pyrimidine salvage pathway in thermophiles: a valuable source of biocatalysts for the industrial production of nucleic acid derivatives vol.102, pp.18, 2017, https://doi.org/10.1007/s00253-018-9242-8
  2. Building a toolbox of protein scaffolds for future immobilization of biocatalysts vol.102, pp.19, 2017, https://doi.org/10.1007/s00253-018-9252-6
  3. The Role of Charged Residues in the Structural Adaptation of Short-Chain Alcohol Dehydrogenase (SDR) from Thermophilic Organisms to High Temperatures vol.73, pp.5, 2018, https://doi.org/10.3103/s0027131418050085
  4. Analysis of the diversity of aerobic, thermophilic endospore-forming bacteria in two Algerian hot springs using cultural and non-cultural methods vol.68, pp.12, 2017, https://doi.org/10.1007/s13213-018-1401-8
  5. Marine enzymes and their industrial and biotechnological applications vol.30, pp.4, 2018, https://doi.org/10.23736/s1120-4826.18.02442-4
  6. Structure and function of the Ts2631 endolysin of Thermus scotoductus phage vB_Tsc2631 with unique N-terminal extension used for peptidoglycan binding vol.9, pp.None, 2019, https://doi.org/10.1038/s41598-018-37417-6
  7. Extremophiles - Platform Strains for Sustainable Production of Polyhydroxyalkanoates vol.955, pp.None, 2017, https://doi.org/10.4028/www.scientific.net/msf.955.74
  8. Editorial: Bioprospecting and Biotechnology of Extremophiles vol.7, pp.None, 2017, https://doi.org/10.3389/fbioe.2019.00204
  9. A polyextremophilic alcohol dehydrogenase from the Atlantis II Deep Red Sea brine pool vol.9, pp.2, 2017, https://doi.org/10.1002/2211-5463.12557
  10. Preparation and evaluation of a polymer–metal–enzyme hybrid nanowire for the immobilization of multiple oxidoreductases vol.94, pp.3, 2017, https://doi.org/10.1002/jctb.5825
  11. Autecology and Hydrolytic Activity of Terrestrial Ecosystems Microorganisms from the Antarctic, Ecuador and Israel vol.81, pp.4, 2017, https://doi.org/10.15407/microbiolj81.04.029
  12. Marine Fungi: Biotechnological Perspectives from Deep-Hypersaline Anoxic Basins vol.11, pp.7, 2017, https://doi.org/10.3390/d11070113
  13. Broadening the Scope of Biocatalysis in Sustainable Organic Synthesis vol.12, pp.13, 2019, https://doi.org/10.1002/cssc.201900351
  14. Tackling the Challenges of Enzymatic (Bio)Fuel Cells vol.119, pp.16, 2017, https://doi.org/10.1021/acs.chemrev.9b00115
  15. Lipases: sources, immobilization methods, and industrial applications vol.103, pp.18, 2019, https://doi.org/10.1007/s00253-019-10027-6
  16. Tandem catalysis in multicomponent solvent-free biofluids vol.11, pp.42, 2017, https://doi.org/10.1039/c9nr06045f
  17. Colombian Andean thermal springs: reservoir of thermophilic anaerobic bacteria producing hydrolytic enzymes vol.23, pp.6, 2017, https://doi.org/10.1007/s00792-019-01132-5
  18. AmyZ1: a novel α-amylase from marine bacterium Pontibacillus sp. ZY with high activity toward raw starches vol.12, pp.None, 2017, https://doi.org/10.1186/s13068-019-1432-9
  19. Computational Analysis of the Primary and Secondary Structure of Amidases in Relation to their pH Adaptation vol.17, pp.2, 2017, https://doi.org/10.2174/1570164616666190718150627
  20. Recent Development of Extremophilic Bacteria and Their Application in Biorefinery vol.8, pp.None, 2017, https://doi.org/10.3389/fbioe.2020.00483
  21. Identification of Proteolytic Thermophiles from Moinit Coastal Hot-Spring, North Sulawesi, Indonesia vol.37, pp.1, 2017, https://doi.org/10.1080/01490451.2019.1662524
  22. Extremophile Microbial Communities and Enzymes for Bioenergetic Application Based on Multi-Omics Tools vol.21, pp.None, 2017, https://doi.org/10.2174/1389202921999200601144137
  23. Wenzhouxiangella Strain AB-CW3, a Proteolytic Bacterium From Hypersaline Soda Lakes That Preys on Cells of Gram-Positive Bacteria vol.11, pp.None, 2020, https://doi.org/10.3389/fmicb.2020.597686
  24. Thermophilic nucleoside phosphorylases: Their properties, characteristics and applications vol.1868, pp.2, 2017, https://doi.org/10.1016/j.bbapap.2019.140304
  25. Xylanases from marine microorganisms: A brief overview on scope, sources, features and potential applications vol.1868, pp.2, 2017, https://doi.org/10.1016/j.bbapap.2019.140312
  26. Deep Hypersaline Anoxic Basins as Untapped Reservoir of Polyextremophilic Prokaryotes of Biotechnological Interest vol.18, pp.2, 2017, https://doi.org/10.3390/md18020091
  27. Modifying Post‐Translational Modifications: A Strategy Used by Archaea for Adapting to Changing Environments? vol.42, pp.3, 2017, https://doi.org/10.1002/bies.201900207
  28. Discovery of hyperstable carbohydrate‐active enzymes through metagenomics of extreme environments vol.287, pp.6, 2017, https://doi.org/10.1111/febs.15080
  29. Glycosidase and Proteolytic Activity of Micromycetes Isolated from the Chernobyl Exclusion Zone vol.82, pp.2, 2017, https://doi.org/10.15407/microbiolj82.02.051
  30. Fungi from the extremes of life: an untapped treasure for bioactive compounds vol.104, pp.7, 2020, https://doi.org/10.1007/s00253-020-10399-0
  31. Genomics of Extremophiles for Sustainable Agriculture and Biotechnological Applications (Part I) vol.21, pp.2, 2017, https://doi.org/10.2174/138920292102200414103212
  32. 16S rRNA Gene Diversity in the Salt Crust of Salar de Uyuni, Bolivia, the World’s Largest Salt Flat vol.9, pp.21, 2017, https://doi.org/10.1128/mra.00374-20
  33. Identification and characterization of the gene encoding an extracellular protease from haloarchaeon Halococcus salifodinae vol.236, pp.None, 2017, https://doi.org/10.1016/j.micres.2020.126468
  34. Microorganisms and Their Metabolic Capabilities in the Context of the Biogeochemical Nitrogen Cycle at Extreme Environments vol.21, pp.12, 2017, https://doi.org/10.3390/ijms21124228
  35. Exploitation of Potential Extremophiles for Bioremediation of Xenobiotics Compounds: A Biotechnological Approach vol.21, pp.3, 2017, https://doi.org/10.2174/1389202921999200422122253
  36. Biocatalysis at Extreme Temperatures: Enantioselective Synthesis of both Enantiomers of Mandelic Acid by Transesterification Catalyzed by a Thermophilic Lipase in Ionic Liquids at 120 °C vol.10, pp.9, 2017, https://doi.org/10.3390/catal10091055
  37. A novel acid‐tolerant β‐xylanase from Scytalidium candidum 3C for the synthesis of o‐nitrophenyl xylooligosaccharides vol.60, pp.11, 2020, https://doi.org/10.1002/jobm.202000303
  38. The Nature of Thermal Stability of Prokaryotic Nucleoside Phosphorylases vol.56, pp.6, 2020, https://doi.org/10.1134/s0003683820060125
  39. Revisiting the scope and applications of food enzymes from extremophiles vol.44, pp.11, 2017, https://doi.org/10.1111/jfbc.13475
  40. Revisiting the scope and applications of food enzymes from extremophiles vol.44, pp.11, 2017, https://doi.org/10.1111/jfbc.13475
  41. Biodiesel and flavor compound production using a novel promiscuous cold-adapted SGNH-type lipase ( Ha SGNH1) from the psychrophilic bacterium Halocynthiibacter arcticus vol.13, pp.None, 2017, https://doi.org/10.1186/s13068-020-01696-x
  42. Structural evidence for kinetic and thermal stability changes of α-amylase due to exposure to [emim][lactate] ionic liquid vol.45, pp.6, 2017, https://doi.org/10.1515/tjb-2019-0270
  43. An Overview of 7α- and 7β-Hydroxysteroid Dehydrogenases: Structure, Specificity and Practical Application vol.28, pp.None, 2017, https://doi.org/10.2174/0929866528666210816114032
  44. Bioprospecting of Novel Extremozymes From Prokaryotes-The Advent of Culture-Independent Methods vol.12, pp.None, 2017, https://doi.org/10.3389/fmicb.2021.630013
  45. Novel Enzymes From the Red Sea Brine Pools: Current State and Potential vol.12, pp.None, 2017, https://doi.org/10.3389/fmicb.2021.732856
  46. Purification and Crystallographic Analysis of a Novel Cold-Active Esterase (HaEst1) from Halocynthiibacter arcticus vol.11, pp.2, 2017, https://doi.org/10.3390/cryst11020170
  47. From Data Mining of Chitinophaga sp. Genome to Enzyme Discovery of a Hyperthermophilic Metallocarboxypeptidase vol.9, pp.2, 2021, https://doi.org/10.3390/microorganisms9020393
  48. Molecules derived from the extremes of life: a decade later vol.38, pp.1, 2017, https://doi.org/10.1039/d0np00021c
  49. M. jannaschii FtsZ, a key protein in bacterial cell division, is inactivated by peroxyl radical-mediated methionine oxidation vol.166, pp.None, 2017, https://doi.org/10.1016/j.freeradbiomed.2021.02.003
  50. Metagenomic Approach to Bacterial Diversity and Lipolytic Enzymes’ Genes from a Steam Soil of Los Humeros Geothermal Field (Puebla, México) vol.38, pp.4, 2017, https://doi.org/10.1080/01490451.2020.1852452
  51. Extremophiles, a Nifty Tool to Face Environmental Pollution: From Exploitation of Metabolism to Genome Engineering vol.18, pp.10, 2021, https://doi.org/10.3390/ijerph18105228
  52. Diversity, Ecological Role and Biotechnological Potential of Antarctic Marine Fungi vol.7, pp.5, 2017, https://doi.org/10.3390/jof7050391
  53. Addressing the Selectivity of Enzyme Biosensors: Solutions and Perspectives vol.21, pp.9, 2017, https://doi.org/10.3390/s21093038
  54. The Molecular Basis for Life in Extreme Environments vol.50, pp.1, 2017, https://doi.org/10.1146/annurev-biophys-100120-072804
  55. Electrostatic interaction optimization improves catalytic rates and thermotolerance on xylanases vol.120, pp.11, 2017, https://doi.org/10.1016/j.bpj.2021.03.036
  56. Titr-DMD-A Rapid, Coarse-Grained Quasi-All-Atom Constant pH Molecular Dynamics Framework vol.17, pp.7, 2017, https://doi.org/10.1021/acs.jctc.1c00338
  57. Biotechnological Conversion of Grape Pomace to Poly(3-hydroxybutyrate) by Moderately Thermophilic Bacterium Tepidimonas taiwanensis vol.8, pp.10, 2017, https://doi.org/10.3390/bioengineering8100141
  58. A Brief History of De Novo Protein Design: Minimal, Rational, and Computational vol.433, pp.20, 2017, https://doi.org/10.1016/j.jmb.2021.167160
  59. Glycoside Hydrolases and Glycosyltransferases from Hyperthermophilic Archaea: Insights on Their Characteristics and Applications in Biotechnology vol.11, pp.11, 2017, https://doi.org/10.3390/biom11111557
  60. Cloning, expression, purification and characterization of chitin deacetylase extremozyme from halophilic Bacillus aryabhattai B8W22 vol.11, pp.12, 2017, https://doi.org/10.1007/s13205-021-03073-3
  61. Lipophilic extracts of the thermophilic cyanobacterium Leptolyngbya sp. and chlorophyte Graesiella sp. and their potential use as food and anticancer agents vol.60, pp.None, 2017, https://doi.org/10.1016/j.algal.2021.102511
  62. Characterization of a thermophilic facultatively anaerobic bacterium Paenibacillus sp. strain DA-C8 that exhibits xylan degradation under anaerobic conditions vol.342, pp.None, 2017, https://doi.org/10.1016/j.jbiotec.2021.10.008
  63. Seawater-based biorefineries: A strategy to reduce the water footprint in the conversion of lignocellulosic biomass vol.344, pp.no.pb, 2017, https://doi.org/10.1016/j.biortech.2021.126325
  64. Purification and Characterization of Strong Simultaneous Enzyme Production of Protease and α-Amylase from an Extremophile-Bacillus sp. FW2 and Its Possibility in Food Waste Degradation vol.8, pp.1, 2017, https://doi.org/10.3390/fermentation8010012
  65. Characterization of the Proteolytic Activity of a Halophilic Aspergillus reticulatus Strain SK1-1 Isolated from a Solar Saltern vol.10, pp.1, 2017, https://doi.org/10.3390/microorganisms10010029