Halophiles pp 421-449 | Cite as

Extracellular Proteases from Halophilic and Haloalkaliphilic Bacteria: Occurrence and Biochemical Properties

  • Vikram H. Raval
  • Megha K. Purohit
  • Satya P. Singh
Chapter
Part of the Sustainable Development and Biodiversity book series (SDEB, volume 6)

Abstract

Polyextremophilic organisms, such as haloalkaliphiles have focused attention due to their hydrolytic enzymes. The halophilic microorganisms include heterotrophic and methanogenic archaea; photosynthetic, lithotrophic, and heterotrophic bacteria; and photosynthetic and heterotrophic eukaryotes. Halophiles and haloalkaliphiles are distributed throughout in hypersaline environments, natural hypersaline brines in arid, coastal, and even deep sea locations, as well as in manmade salterns. The microbes possess range of the biocatalysts which allow them to sustain under the prevailing extreme conditions. Among the enzymes, proteases, carbohydrases, and peroxidases are the most cited candidates. The proteases widely occur in microbial world and play significant role in the processing and maintenance of large number of membrane proteins under the cellular conditions. Besides, the proteases are among the commercially most viable enzymes and dominate the worldwide enzyme market. The proteases of halophilic and haloalkaliphilic bacteria from the marine sources appear to have significant role in the detergent industries, ripening of the salted fish, fish sauces and marinades, modifying fish protein concentrations, dehairing and deskinning, non aqueous enzymology and asymmetric catalysis. In the present chapter, the proteases from the halophilic and haloalkaliphilic bacteria have been reviewed with respect to their occurrence and biochemical properties.

Keywords

Haloalkaliphiles Polyextremophiles Alkaline proteases Halotolerant enzymes Enzyme kinetics Enzyme characterization Biocatalytic potential Metagenomics 
This is a preview of subscription content, log in to check access.

References

  1. Adinarayana K, Ellaiah P, Prasad DS (2003) Purification and partial characterization of thermostable serine alkaline protease from a newly isolated Bacillus subtilis PE-11. AAPS Pharm Scitech 4:1–9Google Scholar
  2. Amoozegar MA, Malekzadeh F, Malik KA, Schumann P, Sproer C (2003) Halobacillus karajensis sp. nov., a novel moderate halophile. Int J Syst Evol Microbiol 53:1059–1063PubMedCrossRefGoogle Scholar
  3. Amoozegar MA, Sanchez-Porro C, Rohban R, Hajighasemi M, Ventosa A (2009) Bacillus persepolensis sp. nov., a moderately halophilic bacterium from a hypersaline lake. Int J Syst Evol Microbiol 59:2352–2358PubMedCrossRefGoogle Scholar
  4. Amoozegar MA, Bagheri M, Makhdoumi-Kakhki A, Didari M, Schumann P, Sproer C, Sanchez-Porro C, Ventosa A (2014) Oceanobacillus limi sp. nov., a moderately halophilic bacterium from a salt lake. Int J Syst Evol Microbiol 64:1284–1289PubMedCrossRefGoogle Scholar
  5. Arahal DR, Garcia MT, Vargas C, Canovas D, Nieto JJ, Ventosa A (2001) Chromohalobacter salexigens sp. nov., a moderately halophilic species that includes Halomonas elongate DSM 3043 and ATCC 33174. Int J Syst Evol Microbiol 51:1457–1462PubMedCrossRefGoogle Scholar
  6. Bagheri M, Didari M, Amoozegar M, Schumann P, Sanchez-Porro C, Mehrshad M, Ventosa A (2012) Bacillus iranensis sp. nov., a moderately halophilic bacterium from Aran-Bidgol Lake, a hypersaline Iranian lake. Int J Syst Evol Microbiol 62(Pt 4):811–816. doi: 10.1099/ijs.0.030874-0 PubMedCrossRefGoogle Scholar
  7. Bagheri M, Amoozegar MA, Didari M, Makhdoumi-Kakhki A, Schumann P, Sproer C, Sanchez-Porro C, Ventosa A (2013) Marinobacter persicus sp. nov., a moderately halophilic bacterium from a saline lake in Iran. Antonie Van Leeuwenhoek 104:47–54PubMedCrossRefGoogle Scholar
  8. Banciu H, Sorokin DY, Galinski EA, Muyzer G, Kleerebezem R, Kuenen JG (2004) Thialkalivibrio halophilus sp. nov., a novel obligately chemolithoautotrophic, facultatively alkaliphilic, and extremely salt-tolerant, sulfur-oxidizing bacterium from a hypersaline alkaline lake. Extremophiles 8:325–334PubMedGoogle Scholar
  9. Battestein V, Macedo GA (2007) Effects of temperature, pH and additives on the activity of tannase produced by Paecilomyces variotii. Electron J Biotechnol 10(2):191–199Google Scholar
  10. Baxter BK, Litchfield CD, Sowers K, Griffith JD, Dassarma PA, Dassarma S (2005) Microbial diversity of Great Salt Lake. In: Adaptation to life at high salt concentrations in archaea, bacteria, and eukarya cellular origin, life in extreme habitats and astrobiology, vol 9. Springer, Dordrecht, pp 9–25Google Scholar
  11. Bayoudh A, Gharsallah N, Chamkha M, Dhouib A, Ammar S, Nasri M (2000) Purification and characterization of an alkaline protease from Pseudomonas aeruginosa MN1. J Ind Microbiol Biotechnol 24:291–295CrossRefGoogle Scholar
  12. Beg KQ, Gupta R (2003) Purification and characterization of an oxidation-stable, thiol-dependent serine alkaline protease from Bacillus mojavensis. Enzyme Microb Technol 32:294–304CrossRefGoogle Scholar
  13. Berezovsky IN, Shakhnovich EI (2008) Physics and evolution of thermophilic adaptation. FEBS J 275(7):1593–1605CrossRefGoogle Scholar
  14. Blum JS, Kulp TR, Han S, Lanoil B, Saltikov CW, Stolz JF, Miller LG, Oremland RS (2012) Desulfohalophilus alkaliarsenatis gen. nov., sp. nov., an extremely halophilic sulfate- and arsenate-respiring bacterium from Searles Lake, California. Extremophiles 16:727–742PubMedCentralPubMedCrossRefGoogle Scholar
  15. Boltianskaia I, Antipov AN, Kolganova TV, Lysenko AM, Kostrikina NA, Zhilina TN (2004) Halomonas campisalis, an obligatorily alkaliphilic, nitrous oxide-reducing denitrifier with a Mo-cofactor-lacking nitrate reductase. Mikrobiologiia 73(3):326–334PubMedGoogle Scholar
  16. Boltyanskaya YV, Kevbrin VV, Lyensko AM, Kolganova TV, Tourova TP, Osipov GA, Zhilina TN (2007) Holomonas mongoliensis sp. nov. and Halomonas kenyensis sp. nov., new haloalkaliphilic denitrifiers capable of N2O reduction, isolated from soda lakes. Microbiology 76:739–747CrossRefGoogle Scholar
  17. Boominadhan U, Rajakumar R, Sivakumaar PKV, Joe MM (2009) Optimization of protease enzyme production using Bacillus sp. isolated from different wastes. Bot Res Int 2(2):83–87Google Scholar
  18. Cabrera A, Aguilera M, Fuentes S, Incerti C, Russell NJ, Ramos-Cormenzana A, Monteoliva-Sanchez M (2007) Halomonas indalinina sp. nov., a moderately halophilic bacterium isolated from a solar saltern in Cabo de Gata, Almeria, southern Spain. Int J Syst Evol Microbiol 57:376–380PubMedCrossRefGoogle Scholar
  19. Carvalho RV, Correa TLR, Matos da Silva JC, Mansur LRC, Martins MLL (2008) Properties of an amylase from thermophilic Bacillus sp. Braz J Microbiol 39(1):102–107PubMedCentralPubMedCrossRefGoogle Scholar
  20. Chand S, Mishra P (2003) Research and application of microbial enzymes. India’s contribution. Adv Biochem Eng Biotechnol 85:95–124PubMedGoogle Scholar
  21. Colquhouna D, Sorumb H (2002) Cloning, characterization and phylogenetic analysis of the fur gene in Vibrio salmonicida and Vibrio logei. Gene 296:213–220CrossRefGoogle Scholar
  22. Corral P, Gutierrez MC, Castillo AM, Dominguez M, Lopalco P, Corcelli A, Ventosa A (2013) Natronococcus roseus sp. nov., a haloalkaliphilic archaeon from a hypersaline lake. Int J Syst Evol Microbiol 63(1):104–108PubMedCrossRefGoogle Scholar
  23. Curtis S (2009) Fermentation of fish soluble proteins, peptides, and amino acids for umami tastes. Food Technol 13:26–30Google Scholar
  24. DasSarma S, Arora P (2001) Halophiles. In: Encyclopedia of life sciences. Macmillan Press, Nature Publishing Group, London, pp 1–9. [WWW document]. http://www.els.net
  25. Demirjian DC, Moris-Varas F, Cassidy CS (2001) Enzymes from extremophiles. Curr Opin Chem Biol 5:144–151PubMedCrossRefGoogle Scholar
  26. Denizci AA, Kazan D, Erarslan A (2010) Bacillus marmarensis sp. nov., an alkaliphilic, protease-producing bacterium isolated from mushroom compost. Int J Syst Evol Microbiol 60:1590–1594. doi: 10.1099/ijs. 0.012369-0 PubMedCrossRefGoogle Scholar
  27. Dobson SJ, James SR, Franzmann PD, McMeekin TA (1990) Emended description of Halomonas halmophila (NCMB 1971T). Int J Syst Bacteriol 40(4):462–463CrossRefGoogle Scholar
  28. Dodia MS (2005) PhD thesis, Saurashtra University, RajkotGoogle Scholar
  29. Dodia MS, Joshi RH, Patel RK, Singh SP (2006) Characterization and stability of extracellular alkaline proteases from moderately halophilic and alkaliphilic bacteria isolated from saline habitat of coastal Gujarat, India. Braz J Microbiol 37:244–252CrossRefGoogle Scholar
  30. Dodia MS, Bhimani HG, Rawal CM, Joshi RH, Singh SP (2008a) Salt dependent resistance against chemical denaturation of alkaline protease from a newly isolated haloalkaliphilic Bacillus sp. Bioresour Technol 99:6223–6227PubMedCrossRefGoogle Scholar
  31. Dodia MS, Rawal CM, Bhimani HG, Joshi RH, Khare SK, Singh SP (2008b) Purification and stability characteristics of an alkaline serine protease from a newly isolated Haloalkaliphilic bacterium sp. AH-6. J Ind Microbiol Biotechnol 35:121–131PubMedCrossRefGoogle Scholar
  32. Doronina NV, Darmaeva T, Trotsenko Y (2003a) Methylophaga natronica sp. nov., a new alkaliphilic and moderately halophilic, restricted-facultatively methylotrophic bacterium from soda lake of the Southern Transbaikal region. J Syst Appl Microbiol 26:382–389CrossRefGoogle Scholar
  33. Doronina NV, Darmaeva TD, Trotsenko YA (2003b) Methylophaga alcalica sp. nov., a novel alkaliphilic and moderately halophilic, obligately methylotrophic bacterium from an East Mongolian saline soda lake. J Syst Evol Microbiol 53(Pt 1):223–229CrossRefGoogle Scholar
  34. Echigo A, Minegishi H, Mizuki T, Kamekura M, Usami R (2010) Geomicrobium halophilum gen. nov., sp. nov., a moderately halophilic and alkaliphilic bacterium isolated from soil. Int J Syst Evol Microbiol 60:990–995PubMedCrossRefGoogle Scholar
  35. Fan H, Xue Y, Ma Y, Ventosa A, Grant WD (2004) Halorubrum tibetense sp. nov., a novel haloalkaliphilic archaeon from Lake Zabuye in Tibet, China. Int J Syst Evol Microbiol 54:1213–1216PubMedCrossRefGoogle Scholar
  36. Feng J, Zhou P, Liu S (2004) Halorubrum xinjiangense sp. nov., a novel halophile isolated from saline lakes in China. Int J Syst Evol Microbiol 54:1789–1791PubMedCrossRefGoogle Scholar
  37. Forsyth MP, Shindler DB, Gochnauer MB, Kushner DJ (2005) Salt tolerance of intertidal marine bacteria. Can J Microbiol 17:825–828CrossRefGoogle Scholar
  38. Foti M, Ma S, Sorokin DY, Rademaker JLW, Kuenen GJ, Muyzer G (2006) Genetic diversity and biogeography of haloalkaliphilic sulfur-oxidizing bacteria belonging to the genus Thioalkalivibrio. FEMS Microbiol Ecol 56:95–101PubMedCrossRefGoogle Scholar
  39. Garcia MT, Gallego V, Ventosa A, Mellado E (2005) Thalassobacillus devorans gen. nov., sp. nov., a moderately halophilic, phenol-degrading, Gram-positive bacterium. Int J Syst Evol Microbiol 55:1789–1795PubMedCrossRefGoogle Scholar
  40. Ghorbel B, Kamoun AS, Nasri M (2003) Stability studies of protease from Bacillus cereus BG1. Enzyme Microb Technol 32:513–518CrossRefGoogle Scholar
  41. Ghosh A, Bhardwaj M, Satyanarayana T, Khurana M, Mayilraj S, Jain RK (2007) Bacillus lehensis sp. nov., an alkalitolerant bacterium isolated from soil. Int J Syst Evol Microbiol 57:238–242PubMedCrossRefGoogle Scholar
  42. Gimenez MI, Studdert CA, Sanchez J, De Castro RE (2000) Extra cellular protease of Natrialba magadii: purification and biochemical characterization. Extremophiles 4:181–188PubMedCrossRefGoogle Scholar
  43. Gonzalez-Domenech CM, Martinez-Checa F, Quesada E, Bejar V (2008) Halomonas cerina sp. nov., a moderately halophilic, denitrifying, exopolysaccharide-producing bacterium. Int J Syst Evol Microbiol 58:803–809PubMedCrossRefGoogle Scholar
  44. Grant WD, Mwatha WE (1998) Bacteria from alkaline, saline environments. In: Hattori T, Ishida Y, Maruyama Y, Morita RY, Uchida A (eds) Recent advances in microbial ecology, vol 1. Japan Scientific Societies Press, Tokyo, pp 29–33Google Scholar
  45. Graziano G, Merlino A (2014) Molecular bases of protein halotolerance. Biochim Biophys Acta (BBA) Protein Proteomics. doi: 10.1016/j.bbapap.2014.02.018 Google Scholar
  46. Gunde-Cimerman N, Zalar P, DeHoog GS, Plementias A (2000) Hypersaline water in salterns. Natural ecological niches for halophilic black yeasts. FEMS Microbiol Ecol 32:235–240Google Scholar
  47. Guo JP, Ying M (2008) High-level expression, purification and characterization of recombinant Aspergillus oryzae alkaline protease in Pichia pastoris. Protein Expr Purif 58(2):301–308PubMedCrossRefGoogle Scholar
  48. Gupta MN, Roy I (2004) Enzymes in organic media forms, functions and applications. Eur J Biochem 271(13):2575–2583PubMedCrossRefGoogle Scholar
  49. Gupta A, Roy I, Patel RK, Singh SP, Khare SK, Gupta MN (2005) One-step purification and characterization of an alkaline protease from haloalkaliphilic Bacillus sp. J Chromatogr A 1075:103–108PubMedCrossRefGoogle Scholar
  50. Hidri DE, Guesmi A, Najjari A, Cherif H, Ettoumi B, Hamdi C, Boudabous A, Cherif A (2013) Cultivation dependant assessment, diversity, and ecology of Haloalkaliphilic bacteria in arid saline systems of southern Tunisia. BioMed Res Int. doi: 10.1155/2013/648141, Article ID 648141, 15PubMedCentralPubMedGoogle Scholar
  51. Hiraga K, Nishikata Y, Namwong S, Tanasupawat S, Takada K, Oda K (2005) Purification and characterization of serine proteinase from a halophilic bacterium, Filobacillus sp. RF2-5. Biosci Biotechnol Biochem 69:38–44PubMedCrossRefGoogle Scholar
  52. Hoover RB, Pikuta EV, Bej AK, Marsic D, Whitman WB, Tang J, Krader P (2003) Spirochaeta americana sp. nov., a new haloalkaliphilic, obligately anaerobic spirochaete isolated from soda Mono Lake in California. Int J Syst Evol Microbiol 53:815–821PubMedCrossRefGoogle Scholar
  53. Horikoshi K (1999) Alkaliphiles: some applications of their products for biotechnology. Microbiol Mol Biol Rev 63:735–750PubMedCentralPubMedGoogle Scholar
  54. Imhoff JF, Sahl HG, Soliman GSH (1979) The Wadi Natrun: chemical composition and microbial mass developments in alkaline brines of Eutrophic Desert Lakes. Geomicrobiol J 1(3):219–234CrossRefGoogle Scholar
  55. James SR, Dobson SJ, Franzmann PD, McMeekin TA (1990) Halomonas meridiana, a new species of extremely halotolerant bacteria isolated from Antarctic saline lakes. Syst Appl Microbiol 13(3):270–278CrossRefGoogle Scholar
  56. Jeon C, Lim J, Lee J, Xu L, Jiang C, Kim C (2005) Reclassification of Bacillus haloalkaliphilus Fritze 1996 as Alkalibacillus haloalkaliphilus gen. nov., comb. nov. and the description of Alkalibacillus salilacus sp. nov., a novel halophilic bacterium isolated from a salt lake in China. Int J Syst Evol Microbiol 55:1891–1896PubMedCrossRefGoogle Scholar
  57. Johnvesly B, Naik GR (2001) Studies on production of thermostable alkaline protease from thermophilic and alkaliphilic Bacillus sp. JB-99 in a chemically defined medium. Process Biochem 37:139–144CrossRefGoogle Scholar
  58. Joo HS, Kumar CG, Park GC, Paik SR, Chang CS (2003) Oxidant and SDS stable alkaline protease from a halo-tolerant Bacillus clausii I-52: production and some properties. J Appl Microbiol 95:267–272PubMedCrossRefGoogle Scholar
  59. Joshi RH (2006) A PhD thesis, Department of Biosciences, Saurashtra University RajkotGoogle Scholar
  60. Joshi RH, Dodia S, Singh SP (2008) Production and optimization of a commercially viable alkaline protease from a haloalkaliphilic bacterium. Biotechnol Bioprocess Eng 13:552–559CrossRefGoogle Scholar
  61. Joshi RH, Dodia MS, Singh SP (2009) Production and optimization of a commercially viable alkaline protease from a haloalkaliphilic bacterium. Biotechnol Bioprocess Eng 13:552–559CrossRefGoogle Scholar
  62. Kamekura M, Seno Y, Holmes ML, Dyall-Smith ML (1992) Molecular cloning and sequencing of the gene for a halophilic alkaline serine protease (halolysin) from an unidentified halophilic archaea strain (172P1) and expression of the gene in Haloferax volcanii. J Bacteriol 174(3):736–742PubMedCentralPubMedGoogle Scholar
  63. Karan R, Khare SK (2011) Stability of haloalkaliphilic Geomicrobium sp. protease modulated by salt. Biochemistry (Moscow) 76:686–693CrossRefGoogle Scholar
  64. Kevbrin VV, Zhilina TN, Rainey FA, Zavarzin GA (1998) Tindallia magadii gen. nov., sp. nov.: an alkaliphilic anaerobic ammonifier from Soda Lake deposits. Curr Microbiol 37:94–100PubMedCrossRefGoogle Scholar
  65. Kim WK, Choi KH, Kim YT, Park HH, Choi JY, Lee YS, Oh HI, Kwon IB, Lee SY (1996) Purification and characterization of a fibrinolytic enzyme produced from Bacillus sp. strain CK11-4 screened from Chungkook-Jang. Appl Environ Microbiol 62:2482–2488PubMedCentralPubMedGoogle Scholar
  66. Kim K, Jin L, Yang H, Lee S (2007) Halomonas gomseomensis sp. nov., Halomonas janggokensis sp. nov., Halomonas salaria sp. nov. and Halomonas denitrificans sp. nov., moderately halophilic bacteria isolated from saline water. Int J Syst Evol Microbiol 57:675–681PubMedCrossRefGoogle Scholar
  67. Kotlova EK, Ivanova NM, Yusupova MP, Voyushina TL, Ivanushkina NE, Chestukhina GG (2007) Thioldependent serine proteinase from Paecilomyces lilacinus purification and catalytic properties. Biochemistry (Moscow) 72:117–123CrossRefGoogle Scholar
  68. Kudrya V, Simonenko I (1994) Alkaline serine proteinase and lectin isolation from the culture fluid of B. subtilis. Appl Microbiol Biotechnol 41:505–509CrossRefGoogle Scholar
  69. Kumar CG, Takagi H (1999) Microbial alkaline proteases: from a bio-industrial view point. Biotechnol Adv 17:561–594PubMedCrossRefGoogle Scholar
  70. Ladenstein R, Antranikian G (1998) Proteins from hyperthermophiles: stability and enzymatic catalysis close to the boiling point of water. Adv Biochem Eng Biotechnol 61:37–85PubMedGoogle Scholar
  71. Li AN, Li DC (2009) Cloning, expression and characterization of the serine protease gene from Chaetomium thermophilum. J Appl Microbiol 106:36–380Google Scholar
  72. Li WJ, Schumann P, Zhang Y, Chen G, Tian X, Xu L, Stackebrandt E, Jiang C (2005) Marinococcus halotolerans sp. nov., isolated from Qinghai, north-west China. Int J Syst Evol Microbiol 55:1801–1804PubMedCrossRefGoogle Scholar
  73. Litchfield CD (2004) Microbial molecular and physiological diversity in hypersaline environments. In: Ventosa A (ed) Halophilic microorganisms. Springer, Berlin/Heidelberg, pp 49–61CrossRefGoogle Scholar
  74. Litchfield CD, Gillevet PM (2002) Microbial diversity and complexity in hypersaline environments: a preliminary assessment. J Ind Microbiol Biotechnol 28:48–55PubMedCrossRefGoogle Scholar
  75. Liu WY, Zeng J, Wang L, Dou YT, Yang SS (2005) Halobacillus dabanensis sp. nov. and Halobacillus aidingensis sp. nov., isolated from salt lakes in Xinjiang. China Int J Syst Evol Microbiol 55:1991–1996PubMedCrossRefGoogle Scholar
  76. Luke KA, Higgins CL, Wittung-Stafshede P (2007) Thermodynamic stability and folding of proteins from hyperthermophilic organisms. FEBS J 274(16):4023–4033PubMedCrossRefGoogle Scholar
  77. Madern D, Ebel C, Zaccai G (2000) Halophilic adaptation of enzymes. Extremophiles 4:91–98PubMedCrossRefGoogle Scholar
  78. Makhdoumi-Kakhki A, Amoozegar MA, Bagheri M, Ramezani M, Ventosa A (2012) Haloarchaeobius iranensis gen. nov., sp. nov., an extremely halophilic archaeon isolated from a saline Lake. Int J Syst Evol Microbiol 62:1021–1026PubMedCrossRefGoogle Scholar
  79. Manni L, Jellouli K, Agrebi R, Bayoudh A, Nasri M (2008) Biochemical and molecular characterization of a novel calcium-dependent metalloprotease from Bacillus cereus SV1. Process Biochem 43(5):522–530CrossRefGoogle Scholar
  80. Margesin R, Schinner F (2001a) Biodegradation and bioremediation of hydrocarbons in extreme environments. Appl Microbiol Biotechnol 56:650–663PubMedCrossRefGoogle Scholar
  81. Margesin R, Schinner F (2001b) Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 5:73–83PubMedCrossRefGoogle Scholar
  82. Martins RF, Davids W, Abu AW, Levander F, Radstrom P, Hatti-Kaul R (2001) Starch-hydrolyzing bacteria from Ethiopian soda lakes. Extremophiles 2:135–144CrossRefGoogle Scholar
  83. Melanie RM, Romine MF, Garcia MT, Antonio V, Bailey TJ, Peyton BM (1999) Halomonas campisalis sp. nov., a denitrifying, moderately Haloalkaliphilic bacterium. Syst Appl Microbiol 22:551–558CrossRefGoogle Scholar
  84. Moreno ML, Perez D, Garcia MT, Mellado E (2013) Halophilic bacteria as a source of novel hydrolytic enzymes. Life 3:38–51. doi: 10.3390/life3010038 CrossRefGoogle Scholar
  85. Mormile MR, Romine MF, Garcia TM, Ventosa A, Bailey T, Peyton BM (1999) Halomonas campisalis sp. nov., a denitrifying, moderately Haloalkaliphilic bacterium system. Appl Microbiol 22:551–558CrossRefGoogle Scholar
  86. Munawar N, Engel PC (2014) Halophilic enzymes: characteristics, structural adaptation and potential applications for biocatalysis. Extremophiles 2(4):334–344Google Scholar
  87. Muntyan MS, Tourova TP, Lysenko AM, Kolganova TV, Fritze D, Skulachev VP (2002) Molecular identification of alkaliphilic and halotolerant strain Bacillus sp. FTU as Bacillus pseudofirmus FTU. Extremophiles 6:195–199PubMedCrossRefGoogle Scholar
  88. Namsaraev Z, Akimov V, Tsapin A, Barinova E, Nealson K, Gorlenko V (2009) Marinospirillum celere sp. nov., a novel haloalkaliphilic, helical bacterium isolated from Mono Lake. Int J Syst Evol Microbiol 59:2329–2332PubMedCrossRefGoogle Scholar
  89. Neklyudov AD, Ivankin AN, Berdutina AV (2000) Properties and uses of protein hydrolysates (review). Appl Biochem Microbiol 36:452–459CrossRefGoogle Scholar
  90. Ni X, Yue L, Chi Z, Li Z, 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
  91. Niehaus F, Bertoldo C, Kahler M, Antranikian G (1999) Extremophiles as a source of novel enzymes for industrial application. Appl Microbiol Biotechnol 51:711–729PubMedCrossRefGoogle Scholar
  92. Nowlan B, Dodia MS, Singh SP, Patel BKC (2006) Bacillus okhensis sp. nov., a halotolerant and alkalitolerant bacterium from an Indian saltpan. Int J Syst Evol Microbiol 56:1073–1077PubMedCrossRefGoogle Scholar
  93. Oberoi R, Beg QK, Puri S, Sazena RK, Gupta R (2001) Characterization and wash performance analysis of an SDS-Stable alkaline protease from Bacillus sp. World J Microbiol Biotechnol 17:493–497CrossRefGoogle Scholar
  94. Oremland RS, Hoeft SE, Santini JM, Bano N, Hollibaugh RA, Hollibaugh JT (2002) Anaerobic oxidation of arsenite in Mono Lake water and by a facultative, arsenite-oxidizing chemoautotroph, strain MLHE-1. Appl Environ Microbiol 68(10):4795–4802PubMedCentralPubMedCrossRefGoogle Scholar
  95. Oren A (2002a) Diversity of halophilic microorganisms: environments, phylogeny, physiology, applications. J Ind Microbiol Biotechnol 28:56–63PubMedCrossRefGoogle Scholar
  96. Oren A (2002b) Halophilic microorganisms and their environments. Kluwer Academic Publishers, Dordrecht. doi: 10.1007/0-306-48053-0 CrossRefGoogle Scholar
  97. Pandey S, Singh SP (2012) Organic solvent tolerance of an α-amylase from haloalkaliphilic bacteria as a function of pH, temperature, and salt concentrations. Appl Biochem Biotechnol 166:1747–1757PubMedCrossRefGoogle Scholar
  98. Pandey S, Rakholiya KD, Raval VH, Singh SP (2012) Catalysis and stability of an alkaline protease from a haloalkaliphilic bacterium under non-aqueous conditions as a function of pH, salt and temperature. J Biosci Bioeng 114(3):251–256PubMedCrossRefGoogle Scholar
  99. Patel RK, Dodia MS, Singh SP (2005) Extracellular alkaline protease from a newly isolated haloalkaliphilic Bacillus sp.: production and optimization. Process Biochem 40:3569–3575CrossRefGoogle Scholar
  100. Patel RK, Dodia MS, Joshi RH, Singh SP (2006a) Production of extracellular haloalkaline protease from a newly isolated haloalkaliphilic Bacillus sp. isolated from sea water in Western India. World J Microbiol Biotechnol 22(4):375–382CrossRefGoogle Scholar
  101. Patel RK, Dodia MS, Joshi RH, Singh SP (2006b) Purification and characterization of alkaline protease from a newly isolated haloalkaliphilic Bacillus sp. Process Biochem 41:2002–2009CrossRefGoogle Scholar
  102. Pesenti PT, Sikaroodi M, Gillevet PM, Sanchez-Porro C, Ventosa A, Litchfield CD (2008) Halorubrum californiense sp. nov., an extreme archaeal halophile isolated from a crystallizer pond at a solar salt plant in California, USA. Int J Syst Evol Microbiol 58:2710–2715PubMedCrossRefGoogle Scholar
  103. Peyton BM (1999) Halomonas campisalis sp. nov., a denitrifying, moderately haloalkaliphilic bacterium. Syst Appl Microbiol 22:551–558PubMedCrossRefGoogle Scholar
  104. Phadatare US, Despande VV, Srinivasan MC (1993) High activity alkaline protease from Conidiobolus coronatus (NCL 86.2.20) enzyme production and compatibility with commercial detergents. Enzyme Microb Technol 15:72–76CrossRefGoogle Scholar
  105. Poli A, Nicolaus B, Denizci A, Yavuzturk B, Kazan D (2013) Halomonas smyrnensis sp. nov., a moderately halophilic, exopolysaccharide-producing bacterium from Camalt Saltern area, Turkey. Int J Syst Evol Microbiol 63:10–18PubMedCrossRefGoogle Scholar
  106. Purohit MK (2012) PhD thesis, Saurashtra University, RajkotGoogle Scholar
  107. Purohit MK, Singh SP (2011) Comparative analysis of enzymatic stability and amino acid sequences of thermostable alkaline proteases from two haloalkaliphilic bacteria isolated from Coastal region of Gujarat, India. Int J Biol Macromol 49:103–112PubMedCrossRefGoogle Scholar
  108. Purohit MK, Singh SP (2014) Cloning, over expression and functional attributes of serine proteases from Oceanobacillus iheyensis O.M.A18 and Haloalkaliphilic bacterium O.M.E12. Process Biochem 49:61–68CrossRefGoogle Scholar
  109. Rahman RNZRA, Geok LP, Basri M, Salleh AB (2006) An organic solvent-stable alkaline protease from Pseudomonas aeruginosa strain K: enzyme purification and characterization. Enzyme Microb Technol 39(7):1484–1491CrossRefGoogle Scholar
  110. Ramesh S, Rajesh M, Mathivanan N (2009) Characterization of a thermostable alkaline protease produced by marine Streptomyces fungicidicus MMLY 614. Bioprocess Biosyst Eng 32:91–800CrossRefGoogle Scholar
  111. Rao MB, Tanksale AM, Ghatge MS, Deshpande VV (1998) Molecular and biotechnological aspects of microbial proteases. Microbiol Mol Biol Rev 62:597–635PubMedCentralPubMedGoogle Scholar
  112. Rattray FP, Bockelmann W, Fox PF (1995) Purification and characterization of an extracellular proteinase from Brevibacterium linens ATCC 9174. Appl Environ Microbiol 61(9):3454–3456PubMedCentralPubMedGoogle Scholar
  113. Raval VH (2013) PhD thesis, Saurashtra University RajkotGoogle Scholar
  114. Raval VH, Pillai S, Rawal CM, Singh SP (2014a) Biochemical and structural characterization of a detergent stable serine alkaline protease from sea water haloalkaliphilic bacteria. Process Biochem 49(6):955–962CrossRefGoogle Scholar
  115. Raval VH, Rawal CM, Bhatt HB, Dahima BR, Pandey S, Singh SP (2014b) Cloning and molecular characterization of a serine protease from sea water haloalkaliphilic bacteria. Ann Microbiol. doi: 10.1007/s13213-014-0869-0 Google Scholar
  116. Rawal CM (2012) PhD thesis, Saurashtra University RajkotGoogle Scholar
  117. Rawal CM, Raval VH, Bhimani HD, Bhensdadiya DV, Kothari CR, Patel AB, Bhatt VD, Parmar NR, Sajnani MR, Koringa PG, Joshi CG, Kothari RK, Singh SP (2012) Whole genome shotgun sequencing of extremophile Alkalibacillus haloalkaliphilus C-5 of Indian origin. J Bacteriol 194(17):4775PubMedCentralPubMedCrossRefGoogle Scholar
  118. Reza H, Heidari K, Amoozegar MA, Hajighasemi M, Ziaee A, Ventosa V (2008) Production, optimization and purification of a novel extracellular, protease from the moderately halophilic bacterium Halobacillus karajensis. J Ind Microbiol Biotechnol 36:21–27Google Scholar
  119. Romano I, Giordano A, Lama L, Nicolaus B, Gambacorta A (2005a) Halomonas campaniensis sp. nov., a haloalkaliphilic bacterium isolated from a mineral pool of Campania Region, Italy. Syst Appl Microbiol 28:610–618PubMedCrossRefGoogle Scholar
  120. Romano I, Lama L, Nicolaus B, Gambacorta A, Giordano A (2005b) Alkalibacillus filiformis sp. nov., isolated from a mineral pool in Campania, Italy. Int J Syst Evol Microbiol 55:2395–2399PubMedCrossRefGoogle Scholar
  121. Romano I, Orlando P, Gambacorta A, Nicolaus B, Dipasquale L, Pascual J, Giordano A, Lama L (2011) Salinivibrio sharmensis sp. nov., a novel haloalkaliphilic bacterium from a saline lake in Ras Mohammed Park (Egypt). Extremophiles 15(2):213–220PubMedCrossRefGoogle Scholar
  122. Rosana HE, Williams H, Kites S, David K (2008) Purification and characterization of Nep proteases from H. volcanii. Prot Exp Purif 43(5):31–37Google Scholar
  123. Rothschild LJ, Manicinelli RL (2001) Life in extreme environments. Nature 409:1092–1101PubMedCrossRefGoogle Scholar
  124. 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 34:111–115PubMedCrossRefGoogle Scholar
  125. Sanchez-Porro C, Mellado E, Bertoldo C, Antranikian G, Ventosa A (2003) Screening and characterization of the protease CP1 produced by the moderately halophilic bacterium Pseudoalteromonas sp. strain CP76. Extremophiles 7:221–228PubMedGoogle Scholar
  126. Sanchez-Porro C, Tokunaga H, Tokunaga M, Ventosa A (2007) Chromohalobacter japonicus sp. nov., a moderately halophilic bacterium isolated from a Japanese salty food. Int J Syst Evol Microbiol 57:2262–2266PubMedCrossRefGoogle Scholar
  127. Sardessai YN, Bhosle S (2004) Industrial potential of organic solvent tolerant bacteria. Biotechnol Prog 20(3):655–660PubMedCrossRefGoogle Scholar
  128. Schiraldi C, De Rosa M (2002) Production of biocatalysts and biomolecules from extremophiles. Trends Biotechnol 20:515–521PubMedCrossRefGoogle Scholar
  129. Setyorini E, Takenaka S, Murakami S, Aoki K (2006) Purification and characterization of two novel halotolerant extracellular proteases from Bacillus subtilis strain FP-133. Biosci Biotechnol Biochem 70(2):433–440PubMedCrossRefGoogle Scholar
  130. Shameer S, Prasada BG, Paramageetham C (2013) Isolation of amylase producing bacteria from solar salterns of Nellore district, Andhra Pradesh, India. RRJMB 2(1):13–16Google Scholar
  131. Shannon JD, Baramova EN, Bajarnason JB, Fox JW (1989) Amino acid sequence of a Crotalus atrox venom metalloproteinase which cleaves type IV collagen and gelatin. J Biol Chem 264(20):11575–11583PubMedGoogle Scholar
  132. Sikkema J, De Bont J, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222PubMedCentralPubMedGoogle Scholar
  133. Sinha R, Srivastava AK, Khare SK (2014) Efficient proteolysis and application of an alkaline protease from halophilic Bacillus sp. EMB9. Prep Biochem Biotechnol 44:680–696PubMedCrossRefGoogle Scholar
  134. Sorokin DY, Kuenen JG (2005) Alkaliphilic chemolithotrophs from soda lakes. FEMS Microbiol Ecol 52:287–295PubMedCrossRefGoogle Scholar
  135. Sorokin DY, Gorlenko VM, Tourova TP, Tsapin AI, Nealson KH, Kuenen JG (2002a) Thialkalimicrobium cyclum sp. nov., and Thialkalivibrio jannaschii sp. nov., new species of alkaliphilic, obligately chemolithoautotrophic sulfur-oxidizing bacteria from a hypersaline alkaline Mono Lake (California). Int J Syst Evol Microbiol 52:657–664PubMedCrossRefGoogle Scholar
  136. Sorokin DY, Tourova TP, Kolganova TV, Sjollema KA, Kuenen G (2002b) Thioalkalispira microaerophila gen. nov., sp. nov., a novel litho autotrophic, sulfur oxidizing bacterium from a soda Lake. Int J Syst Evol Microbiol 52:2175–2182PubMedGoogle Scholar
  137. Sorokin DY, Tourova TP, Lysenko AM, Mityushina LL, Kuenen JG (2002c) Thioalkalivibrio thiocyanoxidans sp. nov., and Thioalkalivibrio paradoxus sp. nov., novel alkaliphilic, obligately autotrophic, sulfur oxidizing bacteria capable of growth on thiocyanate, from soda lakes. Int J Syst Evol Microbiol 52:657–664PubMedCrossRefGoogle Scholar
  138. Sorokin DY, Tourova TP, Antipov AN, Muyzer G, Kuenen JG (2004) Anaerobic growth of the haloalkaliphilic denitrifying sulfur-oxidizing bacterium Thialkalivibrio thiocyanodenitrificans sp. nov., with thiocyanate. Microbiology 150(7):2435–2442PubMedCrossRefGoogle Scholar
  139. Sorokin DY, Zhilina TN, Lysenko AM, Tourova TP, Spiridonova EM (2006) Metabolic versatility of haloalkaliphilic bacteria from soda lakes belonging to the Alkalispirillum-Alkalilimnicola group. Extremophiles 10:213–220PubMedCrossRefGoogle Scholar
  140. Sorokin DY, Tourova TP, Abbas B, Suhacheva MV, Muyzer G (2012) Desulfonatronovibrio halophilus sp. nov., a novel moderately halophilic sulfate-reducing bacterium from hypersaline chloride–sulfate lakes in Central Asia. Extremophiles 16(3):411–417PubMedCentralPubMedCrossRefGoogle Scholar
  141. Taira W, Funatsu Y, Satomi M, Takano T, Abe H (2007) Changes in extractive components and microbial proliferation during fermentation of fish sauce from underutilized fish species and quality of final products. Fish Sci 73:913–923CrossRefGoogle Scholar
  142. Thumar JT, Singh SP (2009) Organic solvent tolerance of an alkaline protease from salt-tolerant alkaliphilic Streptomyces clavuligerus strain Mit-1. J Ind Microbiol Biotechnol 36:211–218PubMedCrossRefGoogle Scholar
  143. Toyokawa Y, Takahara H, Reungsang A, Masakazu F, Yuki H, Tachibana S, Masaaki Y (2010a) Purification and characterization of a halotolerant serine proteinase from thermotolerant Bacillus licheniformis RKK-04 isolated from Thai fish sauce. Appl Microbiol Biotechnol 9:2434–2435Google Scholar
  144. Toyokawa Y, Takahara H, Reungsang A, Masakazu F, Yuki H, Tachibana S, Masaaki Y (2010b) Purification and characterization of a halotolerant serine proteinase from thermotolerant Bacillus licheniformis RKK-04 isolated from Thai fish sauce. Appl Microbiol Biotechnol 86:1867–1875PubMedCrossRefGoogle Scholar
  145. Trigui H, Masmoudi S, Brochier-Armanet C, Maalej S, Dukan S (2011) Characterization of Halorubrum sfaxense sp. nov., a new halophilic archaeon isolated from the solar saltern of Sfax in Tunisia. Int J Microbiol Article ID 240191, 8 pages. doi: 10.1155/2011/240191
  146. Ueda M, Asano T, Nakazawa M, Miyatake K, Inouye K (2008) Purification and characterization of novel raw-starch-digesting and cold-adapted alpha-amylases from Eisenia foetida Comp. Biochem Physiol Mol Biol 150(1):125–130CrossRefGoogle Scholar
  147. Upasani V, Desai S (1990) Sambhar salt lake chemical composition of the brines and studies on haloalkaliphilic archaebacteria. Arch Microb 154:589–593CrossRefGoogle Scholar
  148. Wang Q, Li W, Liu Y, Cao H, Li Z, Guo G (2007) Bacillus qingdaonensis sp. nov., a moderately haloalkaliphilic bacterium isolated from a crude sea-salt sample collected near Qingdao in eastern China. Int J Syst Evol Microbiol 57:1143–1147PubMedCrossRefGoogle Scholar
  149. Wang Q, Hou Y, Xu Z, Miao J, Li G (2008) Optimization of cold-active protease production by the psychrophilic bacterium Colwellia sp., NJ341 with response surface methodology. Bioresour Technol 99(6):1926–1931PubMedCrossRefGoogle Scholar
  150. Watzman H (1997) Left for dead: New Scientist, no. 2068, pp 37–41Google Scholar
  151. Wu G, Wu X, Wang Y, Chi C, Tang Y, Kida K, Wu X, Luan Z (2008) Halomonas daqingensis sp. nov., a moderately halophilic bacterium isolated from an oilfield soil. Int J Syst Evol Microbiol 58:2859–2865PubMedCrossRefGoogle Scholar
  152. Xu X, Wu M, Zhou P, Liu S (2005) Halobiforma lacisalsi sp. nov., isolated from a salt lake in China. Int J Syst Evol Microbiol 55:1949–1952PubMedCrossRefGoogle Scholar
  153. Xu X, Wu Y, Zhou Z, Wang C, Zhou Y, Zhang H, Wang Y, Wu M (2007) Halomonas saccharevitans sp. nov., Halomonas arcis sp. nov. and Halomonas subterranea sp. nov., halophilic bacteria isolated from hypersaline environments of China. Int J Syst Evol Microbiol 57:1619–1624PubMedCrossRefGoogle Scholar
  154. Xue Y, Fan H, Ventosa A, Grant WD, Jones BE, Cowan DA, Ma Y (2005) Halalkalicoccus tibetensis gen. nov., sp. nov., representing a novel genus of haloalkaliphilic archaea. Int J Syst Evol Microbiol 55:2501–2505PubMedCrossRefGoogle Scholar
  155. Xue Y, Ventosa A, Wang X, Ren P, Zhou P, Ma Y (2008) Bacillus aidingensis sp. nov., a moderately halophilic bacterium isolated from Ai-Ding salt lake in China. Int J Syst Evol Microbiol 58:2828–2832PubMedCrossRefGoogle Scholar
  156. Yoon JH, Kang KH, Park YH (2003) Halobacillus salinus sp. nov., isolated from a salt lake on the coast of the East Sea in Korea. Int J Syst Evol Microbiol 53(3):687–693PubMedCrossRefGoogle Scholar
  157. Yoon J, Kang S, Lee S, Lee M, Oh T (2005a) Virgibacillus dokdonensis sp. nov., isolated from a Korean island, Dokdo, located at the edge of the East Sea in Korea. Int J Syst Evol Microbiol 55:1833–1837PubMedCrossRefGoogle Scholar
  158. Yoon J, Lee C, Oh T (2005b) Aeromicrobium alkaliterrae sp. nov., isolated from an alkaline soil, and emended description of the genus Aeromicrobium. Int J Syst Evol Microbiol 55:2171–2175PubMedCrossRefGoogle Scholar
  159. Zhang W, Xue Y, Ma Y, Zhou P, Ventosa A, Grant WD (2002) Salinicoccus alkaliphilus sp. nov., a novel alkaliphile and moderate halophile from Baer Soda Lake in Inner Mongolia Autonomous Region, China. Int J Syst Evol Microbiol 52:789–793PubMedGoogle Scholar
  160. Zhang M, Zhao C, Du L, Lu F, Gao C (2008) Expression, purification, and characterization of a thermophilic neutral protease from Bacillus stearothermophilus in Bacillus subtilis. Sci China Ser C Life Sci J 51(1):52–59CrossRefGoogle Scholar
  161. Zhilina TN, Zavarzin GA, Detkova EN, Rainey FA (1996) Natroniella acetigena gen. nov. sp. nov., an extremely haloalkaliphilic, homoacetic bacterium: a new member of Haloanaerobiales. Curr Microbiol 32(6):320–326PubMedCrossRefGoogle Scholar
  162. Zvereva EA, Fedorova TV, Kevbrin VV (2006) Cellulase activity of a haloalkaliphilic anaerobic bacterium, strain Z-7026. Extremophiles 10(1):53–60PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Vikram H. Raval
    • 1
  • Megha K. Purohit
    • 1
  • Satya P. Singh
    • 1
  1. 1.Department of BiosciencesSaurashtra UniversityRajkotIndia

Personalised recommendations