Characterization of extremely halophilic archaeal isolates from Indian salt pans and their screening for production of hydrolytic enzymes

Akmoussi-Toumi S, Khemili-Talbi S, Ferioune I, Kebbouche-Gana S (2018) Purification and characterization of an organic solvent-tolerant and detergent-stable lipase from Haloferax mediterranei CNCMM 50101. Int J Biol Macromol 116:817–830. https://doi.org/10.1016/j.ijbiomac.2018.05.087 Alsafadi D, Paradisi F (2013) Effect of organic solvents on the activity and stability of halophilic alcohol dehydrogenase (ADH2) from Haloferax volcanii. Extremophiles 17(1):115–122 Anderson I, Scheuner C, Göker M, Mavromatis K, Hooper SD, Porat I, Klenk HP, Ivanova N, Kyrpides N (2011) Novel insights into the diversity of catabolic metabolism from ten haloarchaeal genomes. PLoS One 6(5):e20237 Antunes A, Taborda M, Huber R, Moissl C, Nobre MF, da Costa MS (2008) Halorhabdus tiamatea sp. nov., a non-pigmented, extremely halophilic archaeon from a deep-sea, hypersaline anoxic basin of the Red Sea, and emended description of the genus Halorhabdus. Int J Syst Evolut Microbiol 58(1):215–220 Balkrishna SB (2015) Synthesis of polyhydroxyalkanoates by halophilic archaea and bacteria and their osmoadaptation. Doctoral dissertation, Birla Institute of Technology and Science, Pilani) Bardavid RE, Oren A (2008) Dihydroxyacetone metabolism in Salinibacter ruber and in Haloquadratum walsbyi. Extremophiles 12(1):125–131 BBC Research (2012) In Report BIO030G—Global markets for enzymes in industrial applications. https://www.bccresearch.com/market-research/biotechnology/enzymes-industrial-applications-markets-bio030g.html Birbir M, Calli B, Mertoglu B, Bardavid RE, Oren A, Ogmen MN, Ogan A (2007) Extremely halophilic Archaea from Tuz Lake, Turkey, and the adjacent Kaldirim and Kayacik salterns. World J Microbiol Biotechnol 23(3):309–316 Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(8):911–917 Burns DG, Janssen PH, Itoh T, Kamekura M, Li Z, Jensen G, Dyall-Smith ML (2007) Haloquadratum walsbyi gen. nov., sp. nov., the square haloarchaeon of Walsby, isolated from saltern crystallizers in Australia and Spain. Int J Syst Evolut Microbiol 57(2):387–392 Camacho RM, Mateos JC, González-Reynoso O, Prado LA, Córdova J (2009) Production and characterization of esterase and lipase from Haloarcula marismortui. J Ind Microbiol Biotechnol 36(7):901–909 Chu X, He H, Guo C, Sun B (2008) Identification of two novel esterases from a marine metagenomic library derived from South China Sea. Appl Microbiol Biotechnol 80(4):615–625 Cui HL, Tohty D, Zhou PJ, Liu SJ (2006) Halorubrum lipolyticum sp. nov. and Halorubrum aidingense sp. nov., isolated from two salt lakes in Xin-Jiang, China. Int J Syst Evolut Microbiol 56(7):1631–1634 Cui HL, Lin ZY, Dong Y, Zhou PJ, Liu SJ (2007) Halorubrum litoreum sp. nov., an extremely halophilic archaeon from a solar saltern. Int J Syst Evolut Microbiol 57(10):2204–2206 De Rosa M, Trincone A, Nicolaus B, Gambacorta A (1991) Archaebacteria: lipids, membrane structures, and adaptation to environmental stresses. Life under extreme conditions. Springer, Berlin, Heidelberg, pp 61–87 Dussault HP (1955) An improved technique for staining red halophilic bacteria. J Bacteriol 70(4):484 Dyall-Smith M (2008) The halohandbook: protocols for halobacterial genetics. http://www.haloarchaea.com/resources/halohandbook/index.html. Accessed 31 Aug 2018 Elevi R, Assa P, Birbir M, Ogan A, Oren A (2004) Characterization of extremely halophilic Archaea isolated from the Ayvalik Saltern, Turkey. World J Microbiol Biotechnol 20(7):719–725 Elferink MGL, De Wit JG, Demel R, Driessen AJM, Konings WN (1992) Functional reconstitution of membrane proteins in monolayer liposomes from bipolar lipids of Sulfolobus acidocaldarius. J Biol Chem 267:1375–1381 Fang Z, Li J, Wang Q, Fang W, Peng H, Zhang X, Xiao Y (2014) A novel esterase from a marine metagenomic library exhibiting salt tolerance ability. World J Microbiol Biotechnol 24:771–780 Gattinger A, Günthner A, Schloter M, Munch JC (2003) Characterization of archaea in soils by polar lipid analysis. Eng Life Sci 23(1):21–28 Goh F, Leuko S, Allen MA, Bowman JP, Kamekura M, Neilan BA, Burns BP (2006) Halococcus hamelinensis sp. nov., a novel halophilic archaeon isolated from stromatolites in Shark Bay, Australia. Int J Syst Evolut Microbiol 56(6):1323–1329 Grant WD (2004) Life at low water activity. Philos Trans R Soc Lond B Biol Sci 359(1448):1249–1267 Kakhki AM, Amoozegar MA, Khaledi EM (2011) Diversity of hydrolytic enzymes in haloarchaeal strains isolated from salt lake. Int J Environ Sci Technol 8(4):705–714 Kamekura M (1999) Diversity of members of the family Halobacteriaceae. Microbiol Biogeochem Hypersaline Environ 13:26 Kamekura M, Kates M (1999) Structural diversity of membrane lipids in members of Halobacteriaceae. Biosci Biotechnol Biochem 63(6):969–972 Karan R, Capes MD, Das Sarma S (2012) Function and biotechnology of extremophilic enzymes in low water activity. Aquat Biosyst 8:4 Karray F, Abdallah MB, Kallel N, Hamza M, Fakhfakh M, Sayadi S (2018) Extracellular hydrolytic enzymes produced by halophilic bacteria and archaea isolated from hypersaline lake. Molecular Biology Reports 45(5):1297–1309 Kates M (1977) The phytanyl ether-linked polar lipids and isoprenoid neutral lipids of extremely halophilic bacteria. Prog Chem Fats Other Lipids 15(4):301–342 Kates M (1993) Membrane lipids of archaea. New comprehensive biochemistry, vol 26. Elsevier, Amsterdam, pp 261–295 Kaur S, Purohit MK (2012) Rainfall Statistics of India, Indian Meteorological Department, Ministry of earth sciences. Report number: ESSO/IMD/HS/R.F. REP/02 (2013)/16 Konings WN, Albers SV, Koning S, Driessen AJ (2002) The cell membrane plays a crucial role in survival of bacteria and archaea in extreme environments. Antonie Van Leeuwenhoek 81(1–4):61–72 Kumar S, Karan R, Kapoor S, Singh SP, Khare SK (2012) Screening and isolation of halophilic bacteria producing industrially important enzymes. Braz J Microbiol 43(4):1595–1603 Legat A, Denner E, Dornmayr-Pfaffenhuemer M, Pfeiffer P, Knopf B, Claus H, Stan-Lotter H (2013) Properties of Halococcus salifodinae, an isolate from Permian rock salt deposits, compared with halococci from surface waters. Life 3(1):244–259 Levin L, Herrmann C, Papinutti VL (2008) Optimization of lignocellulolytic enzyme production by the white-rot fungus Trametes trogii in solid-state fermentation using response surface methodology. Biochem Eng J 39(1):207–214 Li X, Yu HY (2014) Characterization of an organic solvent-tolerant lipase from Haloarcula sp. G41 and its application for biodiesel production. Folia Microbiol 59(6):455–463 Litchfield CD, Irby A, Kis-Papo T, Oren A (2000) Comparisons of the polar lipid and pigment profiles of two solar salterns located in Newark, California, USA, and Eilat, Israel. Extremophiles 4(5):259–265 Liu XD, Xu Y (2008) A novel raw starch digesting α-amylase from a newly isolated Bacillus sp. YX-1: purification and characterization. Bioresour Technol 99(10):4315–4320 Madern D, Ebel C, Zaccai G (2000) Halophilic adaptation of enzymes. Extremophiles 4(2):91–98 Mahadik ND, Puntambekar US, Bastawde KB, Khire JM, Gokhale DV (2002) Production of acidic lipase by Aspergillus niger in solid state fermentation. Process Biochem 38(5):715–721 Mani K, Salgaonkar BB, Braganca JM (2012) Culturable halophilic archaea at the initial and crystallization stages of salt production in a natural solar saltern of Goa, India. Aquat Biosyst 8(1):15 Markets and Markets (2014) In Report Code: FB 2277 industrial enzymes market by Types (Carbohydrase, Protease, Lipase), applications (food & beverages, cleaning agents, bio-fuel, animal feed), & Geography—Global Trends & Forecasts to 2018 Markets and Markets (2016) In Report Code: FB 2277 industrial enzymes market by type (Amylases, Cellulases, Proteases, Lipases, and Phytases), application (food and beverages, cleaning agents, and animal feed), source (microorganism, plant, and animal), and Region—Global Forecast to 2022 Martin DD, Ciulla RA, Roberts MF (1999) Osmoadaptation in archaea. Appl Environ Microbiol 65(5):1815–1825 Minegishi H, Echigo A, Nagaoka S, Kamekura M, Usami R (2010) Halarchaeum acidiphilum gen. nov., sp. nov., a moderately acidophilic haloarchaeon isolated from commercial solar salt. Int J Syst Evolut Microbiol 60(11):2513–2516 Moldoveanu N, Kates M, Montero CG, Ventosa A (1990) Polar lipids of non-alkaliphilic Halococci. Biochim Biophys Acta (BBA) Lipids Lipid Metab 1046(2):127–135 Montalvo-Rodriguez RAFAEL, Vreeland RH, Oren A, Kessel M, Betancourt C, López-Garriga JUAN (1998) Halogeometricum borinquense gen. nov., sp. nov., a novel halophilic archaeon from Puerto Rico. Int J Syst Evolut Microbiol 48(4):1305–1312 Moreno ML, Mellado E, Garcia MT, Ventosa A (2007) Diversity of extreme halophiles producing hydrolytic enzymes in hypersaline habitats. Halophiles-2007 booklet, 59–60 Moshfegh M, Shahverdi AR, Zarrini G, Faramarzi MA (2013) Biochemical characterization of an extracellular polyextremophilic α-amylase from the halophilic archaeon Halorubrum xinjiangense. Extremophiles 17:1–11 Müller-Santos M, de Souza EM, Pedrosa FDO, Mitchell DA, Longhi S, Carrière F, Krieger N (2009) First evidence for the salt-dependent folding and activity of an esterase from the halophilic archaea Haloarcula marismortui. Biochim Biophys Acta (BBA) Mol Cell Biol Lipids 1791(8):719–729 Nayek A, Gupta PSS, Banerjee S, Mondal B, Bandyopadhyay AK (2014) Salt-bridge energetics in halophilic proteins. PLoS One 9(4):e93862 Oren A (2010) Industrial and environmental applications of halophilic microorganisms. Environ Technol 31(8–9):825–834 Oren A, Duker S, Ritter S (1996) The polar lipid composition of Walsby’s square bacterium. FEMS Microbiol Lett 138(2–3):135–140 Promchai R, Boonchalearn A, Visessanguan W, Luxananil P (2018) Rapid production of extracellular thermostable alkaline halophilic protease originating from an extreme haloarchaeon, Halobacterium salinarum by recombinant Bacillus subtilis. Biocatal Agric Biotechnol 15:192–198 Rathod BN, Bhatt HH, Upasani VN (2016) Extracellular Hydrolases producing Haloarchaea from Marine Salterns at Okhamadhi, Gujarat, India. Int J Curr Microbiol App Sci 5(11):51–64 Reed CJ, Lewis H, Trejo E, Winston V, Evilia C (2013) Protein adaptations in archaeal extremophiles. Archaea. https://doi.org/10.1155/2013/373275 Rodrigo-Baños M, Garbayo I, Vílchez C, Bonete MJ, Martínez-Espinosa RM (2015) Carotenoids from haloarchaea and their potential in biotechnology. Mar Drugs 13(9):5508–5532 Rohban R, Amoozegar MA, Ventosa A (2009) Screening and isolation of halophilic bacteria producing extracellular hydrolyses from Howz Soltan Lake, Iran. J Ind Microbiol Biot 36(3):333–340 Sánchez-Porro C, Martin S, Mellado E, Ventosa A (2003) Diversity of moderately halophilic bacteria producing extracellular hydrolytic enzymes. J Appl Microbiol 94(2):295–300 Shafiei M, Ziaee AA, Amoozegar MA (2010) Purification and biochemical characterization of a novel SDS and surfactant stable, raw starch digesting, and halophilic α-amylase from a moderately halophilic bacterium, Nesterenkonia sp. strain F. Process Biochem 45(5):694–699 Singh A, Singh AK (2017) Haloarchaea: worth exploring for their biotechnological potential. Biotech Lett 39(12):1793–1800 Sinha R, Khare SK (2012) Characterization of detergent compatible protease of a halophilic Bacillus sp. EMB9: differential role of metal ions in stability and activity. Bioresour Technol 145:357–361 Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739 Thompson DH, Wong KF, Humphry-Baker R, Wheeler JJ, Kim JM, Rananavare SB (1992) Tetraether bolaform amphiphiles as models of archaebacterial membrane lipids: raman spectroscopy, phosphorus-31 NMR, x-ray scattering, and electron microscopy. J Am Chem Soc 114(23):9035–9042 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. https://doi.org/10.1155/2011/240191 Ventosa A, Nieto JJ, Oren A (1998) Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol R 62(2):504–544 Wright AG (2006) Phylogenetic relationships within the order Halobacteriales inferred from 16S rRNA gene sequences. Int J Syst Evol Microbiol 56:1223–1227 Zafrilla B, Martínez-Espinosa RM, Alonso MA, Bonete MJ (2010) Biodiversity of Archaea and floral of two inland saltern ecosystems in the Alto Vinalopó Valley, Spain. Saline Syst 6(1):10 Zhang WJ, Cui HL (2014) Halorubrum salinum sp. nov., isolated from a marine solar saltern. Arch Microbiol 196(6):395–400 Zhang Y, Hao J, Zhang YQ, Chen XL, Xie BB, Shi M, Li PY (2017) Identification and characterization of a novel salt-tolerant esterase from the deep-sea sediment of the South China Sea. Front Microbiol 8:441