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Extremophiles

, Volume 22, Issue 3, pp 335–346 | Cite as

Thermostable marine microbial proteases for industrial applications: scopes and risks

  • Noora Barzkar
  • Ahmad Homaei
  • Roohullah Hemmati
  • Seema Patel
Review

Abstract

Thermostable proteases are important in biotechnological and industrial sectors, due to their stability against denaturing agents and chemicals. The feature that gives them such unique applicability is their reaction at high temperatures, which affords a high concentration of substrate, and less risk of microbial contamination. Nearly 65% of industrial proteases are isolated from marine microbial source, and they can significantly resist a wide range of organic solvents at high temperatures. The most important trait of marine organisms is their adaptability, which allows them to grow optimally in harsh environments such as high salt, temperatures, and pressure—the characteristics of deep-sea hot springs and geothermal sediments. However, proteases are immunogenic, and they can trigger inflammatory conditions in human; so their safety assessment prior to industrial usage is of paramount importance. This review focusses on marine-origin thermophilic proteases, their thermal resistance, scopes of their industrial applications, and risks.

Keywords

Marine microorganisms Thermostable proteases Tailor-made enzymes Industrial applications Immunogenic risks 

Notes

Acknowledgements

The authors would like to declare their appreciation to the research council of the University of Hormozgan. No funding was received for this literature review.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abebe B, Abrham S, Genet A, Hiwot G, Paulos K, Melese A (2014) Isolation, optimization and characterization of protease producing bacteria from soil and water in Gondar town, North West Ethiopia. IJBVI 1:20–24Google Scholar
  2. Abou-Elela GM, Ibrahim HA, Hassan SW, Abd-Elnaby H, El-Toukhy NM (2011) Alkaline protease production by alkaliphilic marine bacteria isolated from Marsa-Matrouh (Egypt) with special emphasis on Bacillus cereus purified protease. Afr J Biotechnol 10:4631–4642Google Scholar
  3. Alain K, Pignet P, Zbinden M, Quillevere M, Duchiron F, Donval J-P, Lesongeur F, Raguenes G, Crassous P, Querellou J (2002) Caminicella sporogenes gen. nov., sp. nov., a novel thermophilic spore-forming bacterium isolated from an East-Pacific Rise hydrothermal vent. Int J Syst Evol Microbiol 52:1621–1628PubMedGoogle Scholar
  4. Alain K, Postec A, Grinsard E, Lesongeur F, Prieur D, Godfroy A (2010) Thermodesulfatator atlanticus sp. nov., a thermophilic, chemolithoautotrophic, sulfate-reducing bacterium isolated from a Mid-Atlantic Ridge hydrothermal vent. Int J Syst Evol Microbiol 60:33–38PubMedCrossRefGoogle Scholar
  5. Ali I, Akbar A, Anwar M, Yanwisetpakdee B, Prasongsuk S, Lotrakul P, Punnapayak H (2014) Purification and characterization of extracellular, polyextremophilic α-amylase obtained from halophilic Engyodontium album. Iran J Biotechnol 12:35–40CrossRefGoogle Scholar
  6. Andrä S, Frey G, Jaenicke R, Stetter KO (1998) The thermosome from Methanopyrus kandleri possesses an NH. es+. rb. ei4. rb-dependent ATPase activity. Eur J Biochem 255:93–99PubMedCrossRefGoogle Scholar
  7. Annamalai N, Rajeswari MV, Thavasi R, Vijayalakshmi S, Balasubramanian T (2013) Optimization, purification and characterization of novel thermostable, haloalkaline, solvent stable protease from Bacillus halodurans CAS6 using marine shellfish wastes: a potential additive for detergent and antioxidant synthesis. Bioprocess Biosyst Eng 36:873–883PubMedCrossRefGoogle Scholar
  8. Annamalai N, Rajeswari MV, Balasubramanian T (2014) Extraction, purification and application of thermostable and halostable alkaline protease from Bacillus alveayuensis CAS 5 using marine wastes. Food Bioprod Process 92:335–342CrossRefGoogle Scholar
  9. Antoine E, Cilia V, Meunier J, Guezennec J, Lesongeur F, Barbier G (1997) Thermosipho melanesiensis sp. nov., a new thermophilic anaerobic bacterium belonging to the order Thermotogales, isolated from deep-sea hydrothermal vents in the southwestern Pacific Ocean. Int J Syst Evol Microbiol 47:1118–1123Google Scholar
  10. Antranikian G, Rüdiger A, Canganella F, Klingeberg M, Sunna A (1995) Biodegradation of polymers at temperatures up to 130 °C. J Macromol Sci Part A Pure Appl Chem 32:661–669CrossRefGoogle Scholar
  11. Anwar A, Saleemuddin M (1998) Alkaline proteases: a review. Biores Technol 64:175–183CrossRefGoogle Scholar
  12. Banerjee UC, Sani RK, Azmi W, Soni R (1999) Thermostable alkaline protease from Bacillus brevis and its characterization as a laundry detergent additive. Process Biochem 35:213–219CrossRefGoogle Scholar
  13. Barrett AJ, Woessner JF, Rawlings ND (2012) Handbook of proteolytic enzymes. Elsevier, AmsterdamGoogle Scholar
  14. Beg QK, Sahai V, Gupta R (2003) Statistical media optimization and alkaline protease production from Bacillus mojavensis in a bioreactor. Process Biochem 39:203–209CrossRefGoogle Scholar
  15. Beygmoradi A, Homaei A (2017) Marine microbes as a valuable resource for brand new industrial biocatalysts. Biocatal Agric Biotechnol 11:131–152Google Scholar
  16. Birrien J-L, Zeng X, Jebbar M, Cambon-Bonavita M-A, Quérellou J, Oger P, Bienvenu N, Xiao X, Prieur D (2011) Pyrococcus yayanosii sp. nov., an obligate piezophilic hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 61:2827–2881PubMedCrossRefGoogle Scholar
  17. Blochl E (1997) Pyrolobus fumarii, gen. and sp. nov., represents and novel group of archaea, extending the upper temperature limit for life to 113 C. Extremophiles 1:14–21PubMedCrossRefGoogle Scholar
  18. Bruins ME, Janssen AE, Boom RM (2001) Thermozymes and their applications. Appl Biochem Biotechnol 90:155–186PubMedCrossRefGoogle Scholar
  19. Burggraf S, Jannasch HW, Nicolaus B, Stetter KO (1990) Archaeoglobus profundus sp. nov., represents a new species within the sulfate-reducing archaebacteria. Syst Appl Microbiol 13:24–28CrossRefGoogle Scholar
  20. Canganella F, Jones WJ, Gambacorta A, Antranikian G (1997) Biochemical and phylogenetic characterization of two novel deep-sea Thermococcus isolates with potentially biotechnological applications. Arch Microbiol 167:233–238PubMedCrossRefGoogle Scholar
  21. Chandrasekaran M, Rajeev Kumar S (2010) Marine microbial enzymes. Biotechnology 9:1–15CrossRefGoogle Scholar
  22. Chellappan S, Jasmin C, Basheer SM, Elyas K, Bhat SG, Chandrasekaran M (2006) Production, purification and partial characterization of a novel protease from marine Engyodontium album BTMFS10 under solid state fermentation. Process Biochem 41:956–961CrossRefGoogle Scholar
  23. Chellappan S, Jasmin C, Basheer SM, Kishore A, Elyas K, Bhat SG, Chandrasekaran M (2011) Characterization of an extracellular alkaline serine protease from marine Engyodontium album BTMFS10. J Ind Microbiol Biotechnol 38:743–752PubMedCrossRefGoogle Scholar
  24. Christie DM, Fisher CR, Lee S-M, Givens S (2006) Back-arc spreading systems: geological, biological, chemical, and physical interactions. American Geophysical Union Geophysical Monograph Series, Washington DC, p 166CrossRefGoogle Scholar
  25. Cowan D (1997) Thermophilic proteins: stability and function in aqueous and organic solvents. Comp Biochem Physiol A Physiol 118:429–438PubMedCrossRefGoogle Scholar
  26. Cowan DA, Daniel RM (1982) The properties of immobilized caldolysin, a thermostable protease from an extreme thermophile. Biotechnol Bioeng 24:2053–2061PubMedCrossRefGoogle Scholar
  27. Cowan D, Daniel R, Morgan H (1985) Thermophilic proteases: properties and potential applications. Trends Biotechnol 3:68–72CrossRefGoogle Scholar
  28. Cui H, Wang L, Yu Y (2015) Production and characterization of alkaline protease from a high yielding and moderately halophilic strain of SD11 marine bacteria. J Chem 2015:1–8CrossRefGoogle Scholar
  29. Dadshahi Z, Homaei A, Zeinali F, Sajedi RH, Khajeh K (2016) Extraction and purification of a highly thermostable alkaline caseinolytic protease from wastes Litopenaeus vannamei suitable for food and detergent industries. Food Chem 202:110–115PubMedCrossRefGoogle Scholar
  30. Dalmaso GZL, Ferreira D, Vermelho AB (2015) Marine extremophiles: a source of hydrolases for biotechnological applications. Mar Drugs 13:1925–1965PubMedPubMedCentralCrossRefGoogle Scholar
  31. de Macario EC, Macario AJ (2000) Stressors, stress and survival; overview. Front Biosci 5:d780–d786PubMedCrossRefGoogle Scholar
  32. De Martin L, Ebert C, Gardossi L, Linda P (2001) High isolated yields in thermolysin-catalysed synthesis of Z-l-aspartyl-l-phenylalanine methyl ester in toluene at controlled water activity. Tetrahedron Lett 42:3395–3397CrossRefGoogle Scholar
  33. Debashish G, Malay S, Barindra S, Joydeep M (2005) Marine enzymes. Adv Biochem Eng Biotechnol 96:189–218PubMedGoogle Scholar
  34. Eggers DK, Valentine JS (2001) Molecular confinement influences protein structure and enhances thermal protein stability. Protein Sci 10:250–261PubMedPubMedCentralCrossRefGoogle Scholar
  35. Eichler J (2001) Biotechnological uses of archaeal extremozymes. Biotechnol Adv 19:261–278PubMedCrossRefGoogle Scholar
  36. Elibol M, Moreira AR (2003) Production of extracellular alkaline protease by immobilization of the marine bacterium Teredinobacter turnirae. Process Biochem 38:1445–1450CrossRefGoogle Scholar
  37. Emi S, Myers DV, Iacobucci GA (1976) Purification and properties of the thermostable acid protease of Penicillium duponti. Biochemistry 15:842–848PubMedCrossRefGoogle Scholar
  38. Erauso G, Reysenbach A-L, Godfroy A, Meunier J-R, Crump B, Partensky F, Baross JA, Marteinsson V, Barbier G, Pace NR (1993) Pyrococcus abyssi sp. nov., a new hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Arch Microbiol 160:338–349CrossRefGoogle Scholar
  39. Fiala G, Stetter KO (1986) Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100 C. Arch Microbiol 145:56–61CrossRefGoogle Scholar
  40. Frappier V, Najmanovich R (2015) Vibrational entropy differences between mesophile and thermophile proteins and their use in protein engineering. Protein Sci 24:474–483PubMedCrossRefGoogle Scholar
  41. Fujiwara S (2002) Extremophiles: developments of their special functions and potential resources. J Biosci Bioeng 94:518–525PubMedCrossRefGoogle Scholar
  42. Fulzele R, DeSa E, Yadav A, Shouche Y, Bhadekar R (2011) Characterization of novel extracellular protease produced by marine bacterial isolate from the Indian Ocean. Braz J Microbiol 42:1364–1373PubMedPubMedCentralCrossRefGoogle Scholar
  43. Gey M, Unger K (1995) Calculation of the molecular masses of two newly synthesized thermostable enzymes isolated from thermophilic microorganisms. J Chromatogr B Biomed Sci Appl 666:188–193CrossRefGoogle Scholar
  44. Giddings L-A, Newman DJ (2015) Bioactive compounds from terrestrial extremophiles In: Bioactive compounds from terrestrial extremophiles. Springer, pp 1–75Google Scholar
  45. Glass JD (1981) Enzymes as reagents in the synthesis of peptides. Enzyme Microb Technol 3:2–8CrossRefGoogle Scholar
  46. Godfroy A, Lesongeur F, Raguénès G, Quérellou J, Antoine E, Meunier J-R, Guezennec J, Barbier G (1997) Thermococcus hydrothermalis sp. nov., a new hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 47:622–626Google Scholar
  47. Goodenough PW, Jenkins JA (1991) Protein engineering to change thermal stability for food enzymes. Biochem Soc Trans 19:655–662PubMedCrossRefGoogle Scholar
  48. Grazú V, Abian O, Mateo C, Batista-Viera F, Fernández-Lafuente R, Guisán JM (2005) Stabilization of enzymes by multipoint immobilization of thiolated proteins on new epoxy-thiol supports. Biotechnol Bioeng 90:597–605PubMedCrossRefGoogle Scholar
  49. Gupta R, Ramnani P (2006) Microbial keratinases and their prospective applications: an overview. Appl Microbiol Biotechnol 70:21–33PubMedCrossRefGoogle Scholar
  50. Gupta R, Beg Q, Lorenz P (2002) Bacterial alkaline proteases: molecular approaches and industrial applications. Appl Microbiol Biotechnol 59:15–32PubMedCrossRefGoogle Scholar
  51. Haddar A, Fakhfakh-Zouari N, Hmidet N, Frikha F, Nasri M, Kamoun AS (2010) Low-cost fermentation medium for alkaline protease production by Bacillus mojavensis A21 using hulled grain of wheat and sardinella peptone. J Biosci Bioeng 110:288–294PubMedCrossRefGoogle Scholar
  52. Haki G, Rakshit S (2003) Developments in industrially important thermostable enzymes: a review. Biores Technol 89:17–34CrossRefGoogle Scholar
  53. Hanzawa S, Hoaki T, Jannasch HW, Maruyama T (1996) An extremely thermostable serine protease from a hyperthermophilic archaeum, Desulfurococcus strain SY, isolated from a deep-sea hydrothermal vent. J Mar Biotechnol 4:121–126Google Scholar
  54. Hartley B (1960) Proteolytic enzymes. Annu Rev Biochem 29:45–72PubMedCrossRefGoogle Scholar
  55. Harzevili FD (2014) Yarrowia lipolytica in biotechnological applications. In: Biotechnological applications of the yeast Yarrowia lipolytica. Springer, pp 17–74Google Scholar
  56. Hasan F, Shah AA, Javed S, Hameed A (2010) Enzymes used in detergents: lipases. Afr J Biotechnol 9:4836–4844Google Scholar
  57. Herbert R, Sharp R (1992) Molecular biology and biotechnology of extremophiles. Blackie & Son Ltd, LondonCrossRefGoogle Scholar
  58. Homaei A (2015a) Enhanced activity and stability of papain immobilized on CNBr-activated sepharose. Int J Biol Macromol 75:373–377PubMedCrossRefGoogle Scholar
  59. Homaei A (2015b) Enzyme Immobilization and its application in the food industry. In: Advances in food biotechnology, p 145Google Scholar
  60. Homaei A (2015c) Purification and biochemical properties of highly efficient alkaline phosphatase from Fenneropenaeus merguiensis brain. J Mol Catal B Enzym 118:16–22CrossRefGoogle Scholar
  61. Homaei A, Etemadipour R (2015) Improving the activity and stability of actinidin by immobilization on gold nanorods. Int J Biol Macromol 72:1176–1181PubMedCrossRefGoogle Scholar
  62. Homaei AA, Sajedi RH, Sariri R, Seyfzadeh S, Stevanato R (2010) Cysteine enhances activity and stability of immobilized papain. Amino Acids 38:937–942PubMedCrossRefGoogle Scholar
  63. Homaei A, Barkheh H, Sariri R, Stevanato R (2014) Immobilized papain on gold nanorods as heterogeneous biocatalysts. Amino Acids 46:1649–1657PubMedCrossRefGoogle Scholar
  64. Homaei A, Ghanbarzadeh M, Monsef F (2016a) Biochemical features and kinetic properties of α-amylases from marine organisms. Int J Biol Macromol 83:306–314PubMedCrossRefGoogle Scholar
  65. Homaei A, Lavajoo F, Sariri R (2016b) Development of marine biotechnology as a resource for novel proteases and their role in modern biotechnology. Int J Biol Macromol 88:542–552PubMedCrossRefGoogle Scholar
  66. Huber R, Woese C, Langworthy TA, Fricke H, Stetter KO (1989) Thermosipho africanus gen. nov., represents a new genus of thermophilic eubacteria within the “Thermotogales”. Syst Appl Microbiol 12:32–37CrossRefGoogle Scholar
  67. Huber H, Hohn MJ, Rachel R, Fuchs T, Wimmer VC, Stetter KO (2002) A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417:63–67PubMedCrossRefGoogle Scholar
  68. Inácio FD, Ferreira RO, Araujo CAVd, Brugnari T, Castoldi R, Peralta RM, Souza CGMd (2015) Proteases of wood rot fungi with emphasis on the genus Pleurotus. BioMed Res Int 2015.  https://doi.org/10.1155/2015/290161
  69. Jackson E, Young L (2001) Ecology and industrial microbiology: learning and earning from diversity. Curr Opin Microbiol 4:281–285CrossRefGoogle Scholar
  70. Jasmin C, Chellappan S, Sukumaran RK, Elyas K, Bhat SG, Chandrasekaran M (2010) Molecular cloning and homology modelling of a subtilisin-like serine protease from the marine fungus, Engyodontium album BTMFS10. World J Microbiol Biotechnol 26:1269–1279PubMedCrossRefGoogle Scholar
  71. Jolivet E, L’Haridon S, Corre E, Forterre P, Prieur D (2003) Thermococcus gammatolerans sp. nov., a hyperthermophilic archaeon from a deep-sea hydrothermal vent that resists ionizing radiation. Int J Syst Evol Microbiol 53:847–851PubMedCrossRefGoogle Scholar
  72. Jones W, Leigh JA, Mayer F, Woese C, Wolfe R (1983) Methanococcus jannaschii sp. nov., an extremely thermophilic methanogen from a submarine hydrothermal vent. Arch Microbiol 136:254–261CrossRefGoogle Scholar
  73. Kashefi K, Lovley DR (2003) Extending the upper temperature limit for life. Science 301:934PubMedCrossRefGoogle Scholar
  74. Khoo TC, Cowan DA, Daniel R, Morgan HW (1984) Interactions of calcium and other metal ions with caldolysin, the thermostable proteinase from Thermus aquaticus strain T351. Biochem J 221:407–413PubMedPubMedCentralCrossRefGoogle Scholar
  75. Kim S-K (2013) Marine microbiology: bioactive compounds and biotechnological applications. Wiley, New YorkCrossRefGoogle Scholar
  76. Kim S-K (2015) Springer handbook of marine biotechnology. Springer, ChamCrossRefGoogle Scholar
  77. Kobayashi T, Kwak YS, Akiba T, Kudo T, Horikoshi K (1994) Thermococcus profundus sp. nov., a new hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Syst Appl Microbiol 17:232–236CrossRefGoogle Scholar
  78. Kumakura M, Kaetsu I, Kobayashi T (1984) Properties of thermolysin immobilized in polymer matrix by radiation polymerization. Enzyme Microb Technol 6:23–26CrossRefGoogle Scholar
  79. Kumar HD (2001) Modern concepts of microbiology. Vikas Publishing House Pvt Ltd, New DelhiGoogle Scholar
  80. Kumar C, Tiwari M, Jany K (1999) Novel alkaline serine proteases from alkalophilic Bacillus spp.: purification and some properties. Process Biochem 34:441–449CrossRefGoogle Scholar
  81. Kumar S, Tsai C-J, Nussinov R (2000) Factors enhancing protein thermostability. Protein Eng 13:179–191PubMedCrossRefGoogle Scholar
  82. Kumar CG, Joo H-S, Koo Y-M, Paik SR, Chang C-S (2004) Thermostable alkaline protease from a novel marine haloalkalophilic Bacillus clausii isolate. World J Microbiol Biotechnol 20:351–357CrossRefGoogle Scholar
  83. Kurr M, Huber R, König H, Jannasch HW, Fricke H, Trincone A, Kristjansson JK, Stetter KO (1991) Methanopyrus kandleri, gen. and sp. nov. represents a novel group of hyperthermophilic methanogens, growing at 110 C. Arch Microbiol 156:239–247CrossRefGoogle Scholar
  84. Kuwabara T, Minaba M, Iwayama Y, Inouye I, Nakashima M, Marumo K, Maruyama A, Sugai A, Itoh T, J-i Ishibashi (2005) Thermococcus coalescens sp. nov., a cell-fusing hyperthermophilic archaeon from Suiyo Seamount. Int J Syst Evol Microbiol 55:2507–2514PubMedCrossRefGoogle Scholar
  85. Kuwabara T, Kawasaki A, Uda I, Sugai A (2011) Thermosipho globiformans sp. nov., an anaerobic thermophilic bacterium that transforms into multicellular spheroids with a defect in peptidoglycan formation. Int J Syst Evol Microbiol 61:1622–1627PubMedCrossRefGoogle Scholar
  86. L’haridon S, Cilia V, Messner P, Raguenes G, Gambacorta A, Sleytr U, Prieur D, Jeanthon C (1998) Desulfurobacterium thermolithotrophum gen. nov., sp. nov., a novel autotrophic, sulphur-reducing bacterium isolated from a deep-sea hydrothermal vent. Int J Syst Evolut Microbiol 48:701–711Google Scholar
  87. Ladero M, Ruiz G, Pessela B, Vian A, Santos A, Garcia-Ochoa F (2006) Thermal and pH inactivation of an immobilized thermostable β-galactosidase from Thermus sp. strain T2: comparison to the free enzyme. Biochem Eng J 31:14–24CrossRefGoogle Scholar
  88. Lasa I, Berenguer J (1993) Thermophilic enzymes and their biotechnological potential. Microbiologia 9:77–89PubMedGoogle Scholar
  89. Lee C-H, Lang J, Yen C-W, Shih P-C, Lin T-S, Mou C-Y (2005) Enhancing stability and oxidation activity of cytochrome c by immobilization in the nanochannels of mesoporous aluminosilicates. J Phys Chem B 109:12277–12286PubMedCrossRefGoogle Scholar
  90. López-García P (1999) DNA supercoiling and temperature adaptation: a clue to early diversification of life? J Mol Evol 49:439–452PubMedCrossRefGoogle Scholar
  91. Mane M, Mahadik K, Kokare C (2013) Purification, characterization and applications of thermostable alkaline protease from marine Streptomyces sp. D1. Int J Pharm Bio Sci 4:572–582Google Scholar
  92. Marrs B, Delagrave S, Murphy D (1999) Novel approaches for discovering industrial enzymes. Curr Opin Microbiol 2:241–245PubMedCrossRefGoogle Scholar
  93. Marteinsson VT (1999) Isolation and characterization of Thermus thermophilus Gy1211 from a deep-sea hydrothermal vent. Extremophiles 3:247–251PubMedCrossRefGoogle Scholar
  94. Maruthiah T, Somanath B, Immanuel G, Palavesam A (2015) Deproteinization potential and antioxidant property of haloalkalophilic organic solvent tolerant protease from marine Bacillus sp. APCMST-RS3 using marine shell wastes. Biotechnol Rep 8:124–132CrossRefGoogle Scholar
  95. Maruthiah T, Somanath B, Jasmin JV, Immanuel G, Palavesam A (2016) Production, purification and characterization of halophilic organic solvent tolerant protease from marine crustacean shell wastes and its efficacy on deproteinization. 3 Biotech 6:157PubMedPubMedCentralCrossRefGoogle Scholar
  96. McDonald JH (2010) Temperature adaptation at homologous sites in proteins from nine thermophile–mesophile species pairs. Genome Biol Evol 2:267–276PubMedPubMedCentralCrossRefGoogle Scholar
  97. Menéndez-Arias L, Argosf P (1989) Engineering protein thermal stability: sequence statistics point to residue substitutions in α-helices. J Mol Biol 206:397–406PubMedCrossRefGoogle Scholar
  98. Morikawa M, Izawa Y, Rashid N, Hoaki T, Imanaka T (1994) Purification and characterization of a thermostable thiol protease from a newly isolated hyperthermophilic Pyrococcus sp. Appl Environ Microbiol 60:4559–4566PubMedPubMedCentralGoogle Scholar
  99. Ni X, Chi Z, Ma C, Madzak C (2008) Cloning, characterization, and expression of the gene encoding alkaline protease in the marine yeast Aureobasidium pullulans 10. Mar Biotechnol 10:319–327PubMedCrossRefGoogle Scholar
  100. Ni X, Yue L, Chi Z, Li J, Wang X, Madzak C (2009) Alkaline protease gene cloning from the marine yeast Aureobasidium pullulans HN2-3 and the protease surface display on Yarrowia lipolytica for bioactive peptide production. Mar Biotechnol 11:81–89PubMedCrossRefGoogle Scholar
  101. Niehaus F, Bertoldo C, Kähler M, Antranikian G (1999) Extremophiles as a source of novel enzymes for industrial application. Appl Microbiol Biotechnol 51:711–729PubMedCrossRefGoogle Scholar
  102. Norde W, Zoungrana T (1998) Surface-induced changes in the structure and activity of enzymes physically immobilized at solid/liquid interfaces. Biotechnol Appl Biochem 28:133–143PubMedGoogle Scholar
  103. Nunoura T, Oida H, Miyazaki M, Suzuki Y, Takai K, Horikoshi K (2007) Desulfothermus okinawensis sp. nov., a thermophilic and heterotrophic sulfate-reducing bacterium isolated from a deep-sea hydrothermal field. Int J Syst Evol Microbiol 57:2360–2364PubMedCrossRefGoogle Scholar
  104. Ohta Y (1967) Thermostable protease from thermophilic bacteria II. Studies on the stability of the protease. J Biol Chem 242:509–515PubMedGoogle Scholar
  105. Ong PS, Gaucher GM (1976) Production, purification and characterization of thermomycolase, the extracellular serine protease of the thermophilic fungus Malbranchea pulchella var. sulfurea. Can J Microbiol 22:165–176PubMedCrossRefGoogle Scholar
  106. Pantazaki A, Pritsa A, Kyriakidis D (2002) Biotechnologically relevant enzymes from Thermus thermophilus. Appl Microbiol Biotechnol 58:1–12PubMedCrossRefGoogle Scholar
  107. Patel S (2017a) A critical review on serine protease: key immune manipulator and pathology mediator. Allergol Immunopathol 45(6):579–591.  https://doi.org/10.1016/j.aller.2016.10.011 CrossRefGoogle Scholar
  108. Patel S (2017b) Pathogenicity-associated protein domains: the fiercely-conserved evolutionary signatures. Gene Rep 7:127–141.  https://doi.org/10.1016/j.genrep.2017.04.004 CrossRefGoogle Scholar
  109. Patel S, Rauf A, Meher BR (2017) In silico analysis of ChtBD3 domain to find its role in bacterial pathogenesis and beyond. Microb Pathog 110:519–526PubMedCrossRefGoogle Scholar
  110. Potumarthi R, Ch S, Jetty A (2007) Alkaline protease production by submerged fermentation in stirred tank reactor using Bacillus licheniformis NCIM-2042: effect of aeration and agitation regimes. Biochem Eng J 34:185–192CrossRefGoogle Scholar
  111. Prakash M, Banik RM, Koch-Brandt C (2005) Purification and characterization of Bacillus cereus protease suitable for detergent industry. Appl Biochem Biotechnol 127:143–155PubMedCrossRefGoogle Scholar
  112. Ramesh S, Rajesh M, Mathivanan N (2009) Characterization of a thermostable alkaline protease produced by marine Streptomyces fungicidicus MML1614. Bioprocess Biosyst Eng 32:791–800PubMedCrossRefGoogle Scholar
  113. Rao MB, Tanksale AM, Ghatge MS, Deshpande VV (1998a) Molecular and biotechnological aspects of microbial proteases. Microbiol Mol Biol Rev 62:597–635PubMedPubMedCentralGoogle Scholar
  114. Rao SV, Anderson KW, Bachas LG (1998b) Oriented immobilization of proteins. Microchim Acta 128:127–143CrossRefGoogle Scholar
  115. Roche RS, Voordouw G, Matthews BW (1978) The structural and functional roles of metal ions in thermolysin. CRC Crit Rev Biochem 5:1–23PubMedCrossRefGoogle Scholar
  116. Russell RJ, Gerike U, Danson MJ, Hough DW, Taylor GL (1998) Structural adaptations of the cold-active citrate synthase from an Antarctic bacterium. Structure 6:351–361PubMedCrossRefGoogle Scholar
  117. Sako Y, Nakagawa S, Takai K, Horikoshi K (2003) Marinithermus hydrothermalis gen. nov., sp. nov., a strictly aerobic, thermophilic bacterium from a deep-sea hydrothermal vent chimney. Int J Syst Evol Microbiol 53:59–65PubMedCrossRefGoogle Scholar
  118. Salleh A, Basri M, Razak C (1977) The effect of temperature on the protease from Bacillus stearothermophilus strain F1. Mal J Biochem Mol Biol 2:37–41Google Scholar
  119. Sana B, Ghosh D, Saha M, Mukherjee J (2006) Purification and characterization of a salt, solvent, detergent and bleach tolerant protease from a new gamma-Proteobacterium isolated from the marine environment of the Sundarbans. Process Biochem 41:208–215CrossRefGoogle Scholar
  120. Sanman LE, Bogyo M (2014) Activity-based profiling of proteases. Annu Rev Biochem 83:249–273PubMedCrossRefGoogle Scholar
  121. Segerer AH, Burggraf S, Fiala G, Huber G, Huber R, Pley U, Stetter KO (1993) Life in hot springs and hydrothermal vents. Orig Life Evol Biosph 23:77–90PubMedCrossRefGoogle Scholar
  122. Shanmugavel M, Vasantharaj S, Saathiyavimal S, Gnanamani A (2016) Application of an alkaline protease in biological waste processing: an eco-friendly approach. Int J Biosci Nanosci (IJBSANS) 3:19–24Google Scholar
  123. Sievert SM, Kuever J (2000) Desulfacinum hydrothermale sp. nov., a thermophilic, sulfate-reducing bacterium from geothermally heated sediments near Milos Island (Greece). Int J Syst Evol Microbiol 50:1239–1246PubMedCrossRefGoogle Scholar
  124. Simpson HD, Haufler UR, Daniel RM (1991) An extremely thermostable xylanase from the thermophilic eubacterium Thermotoga. Biochem J 277:413–417PubMedPubMedCentralCrossRefGoogle Scholar
  125. Slobodkina G, Kolganova T, Tourova T, Kostrikina N, Jeanthon C, Bonch-Osmolovskaya E, Slobodkin A (2008) Clostridium tepidiprofundi sp. nov., a moderately thermophilic bacterium from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 58:852–855PubMedCrossRefGoogle Scholar
  126. Sokolova T, Gonzalez J, Kostrikina N, Chernyh N, Tourova T, Kato C, Bonch-Osmolovskaya E, Robb F (2001) Carboxydobrachium pacificum gen. nov., sp. nov., a new anaerobic, thermophilic, CO-utilizing marine bacterium from Okinawa Trough. Int J Syst Evol Microbiol 51:141–149PubMedCrossRefGoogle Scholar
  127. Sookkheo B, Sinchaikul S, Phutrakul S, Chen S-T (2000) Purification and characterization of the highly thermostable proteases from Bacillus stearothermophilus TLS33. Protein Expr Purif 20:142–151PubMedCrossRefGoogle Scholar
  128. Souza PMd, Bittencourt MLdA, Caprara CC, Freitas Md, Almeida RPCd, Silveira D, Fonseca YM, Ferreira Filho EX, Pessoa Junior A, Magalhães PO (2015) A biotechnology perspective of fungal proteases. Braz J Microbiol 46:337–346PubMedPubMedCentralCrossRefGoogle Scholar
  129. Srinivasan M, Rele MV (1999) Microbial xylanases for paper industry. Curr Sci 77:137–142Google Scholar
  130. Sterner Rh, Liebl W (2001) Thermophilic adaptation of proteins. Crit Rev Biochem Mol Biol 36:39–106PubMedCrossRefGoogle Scholar
  131. Synowiecki J, Porta R, Pierro PD, Mariniello L (2008) Thermostable enzymes in food processing. In: Enzymes as additives or processing aids, pp 29–54Google Scholar
  132. Takai K, Sugai A, Itoh T, Horikoshi K (2000) Palaeococcus ferrophilus gen. nov., sp. nov., a barophilic, hyperthermophilic archaeon from a deep-sea hydrothermal vent chimney. Int J Syst Evol Microbiol 50:489–500PubMedCrossRefGoogle Scholar
  133. Trincone A (2013) Biocatalytic processes using marine biocatalysts: ten cases in point. Curr Org Chem 17:1058–1066CrossRefGoogle Scholar
  134. Turk B, Turk D, Turk V (2012) Protease signalling: the cutting edge. EMBO J 31:1630–1643PubMedPubMedCentralCrossRefGoogle Scholar
  135. Unsworth LD, van der Oost J, Koutsopoulos S (2007) Hyperthermophilic enzymes—stability, activity and implementation strategies for high temperature applications. FEBS J 274:4044–4056PubMedCrossRefGoogle Scholar
  136. Vertriani C, Speck M, Ellor S, Lutz R, Starovoytov V (2003) Thermovibrio ammoniificans sp. nov., a thermophilic, chemolithotrophic, nitrate ammonifying bacterium from deep-sea hydrothermal vents. Int J Syst Evol Microbiol 54:175–181CrossRefGoogle Scholar
  137. Vieille C, Zeikus GJ (2001) Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol Mol Biol Rev 65:1–43PubMedPubMedCentralCrossRefGoogle Scholar
  138. Wang S-L, Yeh P-Y (2006) Production of a surfactant-and solvent-stable alkaliphilic protease by bioconversion of shrimp shell wastes fermented by Bacillus subtilis TKU007. Process Biochem 41:1545–1552CrossRefGoogle Scholar
  139. Wang S-L, Chio Y-H, Yen Y-H, Wang C-L (2007) Two novel surfactant-stable alkaline proteases from Vibrio fluvialis TKU005 and their applications. Enzyme Microb Technol 40:1213–1220CrossRefGoogle Scholar
  140. Wery N, Lesongeur F, Pignet P, Derennes V, Cambon-Bonavita M-A, Godfroy A, Barbier G (2001) Marinitoga camini gen. nov., sp. nov., a rod-shaped bacterium belonging to the order Thermotogales, isolated from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 51:495–504PubMedCrossRefGoogle Scholar
  141. Zeinali F, Homaei A, Kamrani E (2015) Sources of marine superoxide dismutases: characteristics and applications. Int J Biol Macromol 79:627–637PubMedCrossRefGoogle Scholar
  142. Zhan D, Sun J, Feng Y, Han W (2014) Theoretical study on the allosteric regulation of an oligomeric protease from Pyrococcus horikoshii by Cl ion. Molecules 19:1828–1842PubMedCrossRefGoogle Scholar
  143. Zhao H, Wood AG, Widdel F, Bryant MP (1988) An extremely thermophilic Methanococcus from a deep sea hydrothermal vent and its plasmid. Arch Microbiol 150:178–183CrossRefGoogle Scholar
  144. Zuber H (1988) Temperature adaptation of lactate dehydrogenase structural, functional and genetic aspects. Biophys Chem 29:171–179PubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Noora Barzkar
    • 1
  • Ahmad Homaei
    • 2
    • 5
  • Roohullah Hemmati
    • 3
  • Seema Patel
    • 4
  1. 1.Department of Marine Biology, Faculty of Marine Science and TechnologyUniversity of HormozganBandar AbbasIran
  2. 2.Department of Biochemistry, Faculty of SciencesUniversity of HormozganBandar AbbasIran
  3. 3.Department of Biology, Faculty of Basic SciencesShahrekord UniversityShahrekordIran
  4. 4.Bioinformatics and Medical Informatics Research CenterSan Diego State UniversitySan DiegoUSA
  5. 5.Department of Biology, Faculty of SciencesUniversity of HormozganBandar AbbasIran

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