sign in sign up
<<
Home , Halophile

Int.J.Curr.Microbiol.App.Sci (2015) 4(12): 616-629

ISSN: 2319-7706 Volume 4 Number 12 (2015) pp. 616-629 http://www.ijcmas.com

Review Article Halophiles-A Review

Deepa Yadav*, Anuradha Singh and Nupur Mathur

Department of Zoology University of Rajasthan, Jaipur- 302004, India *Corresponding author

A B S T R A C T

K e y w o r d s , able to live in unusual habitats can serve as a potential source of novel and their metabolites gain diverse applications and thus Extremophiles, these microorganisms are extensively studied. Halophiles are a group of Halophiles, microorganisms that live in saline environments and in many cases require saline to survive. Hypersaline habitats are tremendous sources of halophilic environments, microorganisms and studies of these microorganisms are of special importance as they are capable of producing compounds of diverse industrial, pharmaceutical and biomedical potentials.

Introduction

Extremophiles are those microorganisms concentrations. These microorganisms which require extreme environment for inhabit the world s most saline growth. The term was first environments, like hypersaline lake, solar used by MacElroy in 1974. Extreme , evaporation pond, flats and tidal environment is a relative term, since marine environments. Halophilic environments that are extreme for one have the capacity to balance the osmotic organism may be essential for the survival pressure of the environment and resist the of another organism. Extremolphiles are denaturing effects of . On the basis of those microorganism which live in extreme their or optimum salt environment like high or low temperature, concentration wherein these organisms grow salt concentration, pH etc. Extremophiles they are categorized as slight (2-5% NaCl), live under conditions that would kill most moderate (5-15% NaCl) or extreme other creatures and many cannot survive in halophiles (15-30% NaCl). the normal global conditions. On the bases of their habitation these extremophiles can To survive in higher saline environment be categorized as: , alkalophiles, halophilic microorganisms use different halophiles, and . types of strategies, they synthesize Among extremophiles halophiles are those compatible solutes in cells or possess the which are able to survive in high salt transporters that help them to survive in

616

Int.J.Curr.Microbiol.App.Sci (2015) 4(12): 616-629 such type of harsh condition. work in such type of saline conditions. Osmoregulatory solutes such as These properties can be used for the ion, glutamate, proline, ectoine and development of techniques outlined have been reported in these bacteria essentially on the optimal condition of these (Madigan, 1999 and Galinski, 1993). Some biomolecules. halophiles produce acidic proteins that have the capacity to function in high salt These properties could be exploited for the concentration. development of additional bio-industrial processes based on the optimal conditions of these biomolecules. To cope up with the high and often changing salinity of their Examples of well adapted and widely environment, the aerobic halophilic bacteria, similar to all other microorganisms, need to balance their cytoplasm with the osmotic distributed extremely halophilic pressure exerted by the external medium microorganisms include for example (Madigan, 1999;Oren, 2008; Oren, 2010).

Important Characteristics Of Halophiles sp. NRC 1, cyanobacteria Enzymes such as Aphanothece halophytica and the Enzymes are catalysts which have potential green alga Dunaliella salina. Multicellular applications in food, detergent formulations, halophilic eukaryotic organisms include metal recovery, leather processing and in brine shrimp and the larvae of brine flies. several industries. Extremophile enzymes, especially extracellular, have been found to Occurence and Distribution have potential industrial applications as they can survive and catalyze reactions in Halophiles can be found in areas where the unusual environment. concentration of salt is five times greater than that salt concentration of the ocean. Table 1 has listed different isolation sites Saline and hypersaline environments are from where halophilic microorganisms have broadly dispersed all through world either been isolated and different enzymes which salt lakes (The , The Great Salt are assayed. Lakes etc.) or salt mines [Salzbad-Salzetnan (Austria), Slanic, Turda, Praid (Romania), Nucleases Wieliczka (Poland), Nakhlichevan (Azerbaidjan), Chon-Tous (Kirghizstan), A nuclease (nuclease H) is reported from Cave Berezniki in Perm(Russia), Solotvino M. varians subsp. halophilus having both (Ukraine) etc.]. These hypersaline DNase and RNase activities. Another environments are too harsh for normal life to halophilic nuclease (an exonuclease, exist, but a variety of microbessurvive. releasing 5 -mononucleotides from both DNA and RNA) was produced by Bacillus These microorganisms produce different halophilus (Onishiet al.,1983). bioactive compounds like enzymes, pigments, solutes, metabolites and Amylases exopolysaccharides which have the ability to

617 Int.J.Curr.Microbiol.App.Sci (2015) 4(12): 616-629

In recent years, a number of studies have A few -amylases were purified and been conducted to characterize extracellular characterized from halophilic proteases from Salinivibrio genus (Lama et microorganisms, Acinetobacter (Onishiet al.,2005 and Amoozegar et al., 2007), al., 1980), Pseudoalteromonas sp. strain CP76 (Goodand Hartman1970, Patel et al., 1993), (Sa´nchez-Porro et al., 2003), M. varians subsp. halophilus (Kobayashiet magadii (Gime´nez et al., 2000), al., 1986), N. halobia (Onishiet al., 1991), Halobacterium mediterranei (Stepanov et Natronococcus amylolyticus (Kobayashi et al. 1992), Bacillus clausii (Kumar et al. al., 1992), (Coronado 2004). There is also a report that a et al., 2000), Haloferax mediterranei (Perez- chymotrypsinogen B-like protease was Pomares et al., 2003)etc. isolated from the haloalkaliphilic archaeon Natronomonas pharaonis (Stan-Lotteret al., The enzyme from sp. S-1 1999). showed high tolerance to various organic solvents (Fukushima et al., 2005). The effect Lipases of ionic strength on the amylase activity, has also been reported at various ratios of Na+ Lipase is one of the most important and Mg2+ concentrations (Enache et al., hydrolytic enzymes with potential in various 2009). fields of pharmaceutical industry and agriculture. Various moderately or Proteases extremely halophilic microorganisms have been reported for the production of lipase Halophilic microorganisms produce which are also stable at high temperature - proteases which can have novel applications Salinivibrio sp. (Amoozegar et al., 2008), (Margesin et al., 2001) because of its high Natronococcus sp. (Boutaiba et al., 2006), stability at saturated salt concentrations or haloarchaeal strains (Ozcan et al., 2009) etc. organic solvent tolerance. Cellulose-Degrading Enzymes Halobacterium salinarum (Ryu et al., 1994) produce an extra cellular serine protease that Bolobova et al., (1992) first reported a has potential to be used for peptide cellulose-utilizing, extremely halophilic synthesis. The other serine proteases were bacterium. The obligate anaerobic organism isolated from Natronococcu soccultus named Halocella cellulolytica is able to (Studdert et al.,1997), Natronomonas utilize cellulose as a sole carbon source. pharaonis (Stan-Lotter et al., 1999), Natrial Another work has shown that many bamagadii (Gimenez et al.,2000). Some cellulose-utilizing extremely halophilic other proteases were purified and Archaea are present in subsurface salt characterized from Natrial baasiatica formation (Vreeland et al.,1998). A (Kamekura et al., 1992) and Haloferax preliminary work done by Cojoc et al., mediterranei (Kamekura et al,1992 and (2009) on extracellular hydrolytic enzymes Kamekura et al.,1996) and other halophilic of halophilic microorganisms from isolates (Norberg and Hofsten, 1969; subterranean rock salt revealed the presence Kamekura and Onishi, 1974; Kamekura and of cellulose. Seno, 1990). Pigments

618 Int.J.Curr.Microbiol.App.Sci (2015) 4(12): 616-629

erythromycin and gentamycin which used to Halophilic microorganisms are a great be one of the important cures are now less source of diverse natural products. effective because bacteria have become Carotenoid pigments are one of these natural more resistant. products responsible for the yellow, orange, red, and purple colors in a wide variety of Halophilic bacteria isolated from different plants, animals, and microorganisms (Li Z et region were found resistant against different al.,2012 and Cabral et al.,2011).Carotenoid antibiotics :Halobactericeae (Hilpert, 1981), pigments are particularly prominent in Halomonas elongate (Boneloet al., 1984), hypersaline environment. Red and orangish Bacillus cereus SIU1 (Singhet al., 2010). color of hypersaline habitats is due to the presence of pigmented microorganisms, Antimicrobial Activity including Dunaliella, rich in -carotene, whose main production is Foreshore soil of Daecheon Beach and bacterioruberin, and halophilic bacteria, Saemangeum Sea of Korea represents an such as producing a untapped source of bacterial biodiversity carotenoid called salinixanthin (El-Banna and also that most actinobacterial isolates Aaet al.,2012 and Jehlicka et al., 2013). An are capable of antibacterial and antifungal extremely halophilic archaeon isolated from metabolite production. The halophiles Urmia Lake, sp. TBZ126 is isolated from Ratnagiri coastal area (marine reported as potential producer of carotenoids environments) having antibacterial and (Naziri et al.,2014). antifungal activity. The antibacterial and antifungal assays of halophiles (protein Melanin is nearly a ubiquitous pigment crude extract) have shown that, the marine having immense application potentials in the environments represent a potential source of field of agriculture, cosmetics and new antimicrobial and antifungal agents pharmaceutical industries (photoprotection (Todkar et al., 2012). and mosquitocidal activity isolated from Streptomycete). Rani et al.,(2013) reported a Microbacterium oxydans and Streptomyces halophilic black , fradiae showed anibactrialactivity against all which produced a diffusible dark pigment on tested pathogenic bacteria and (Irshad potato dextrose agar. It also showed et al., 2013).Sawale et al., (2014) collected inhibitory activity against potential soil samples from coastal area of Arabic pathogens and activity was observed in ocean (Mumbai) and reported antibiotics Salmonella typhi and Vibrio production from two bacterial strains parahaemolyticus. Bacillus pumilus (NKCM 8905) and Bacillus pumilus (AB211228). Resistance to Antibiotics Applications The emergence of antibiotic resistance is an evolutionary process that is based on Biotechnological Application selection for organisms that have enhanced ability to survive doses of antibiotics that Moderately halophilic bacteria have the would have previously been lethal (Cowen, potential for exciting and promising 2008). Pearson and Carol (2008) reported applications. Not only do many of them different antibiotics likes penicillin, produce compounds of industrial interest

619 Int.J.Curr.Microbiol.App.Sci (2015) 4(12): 616-629

(enzymes, polymers and osmoprotectants), coccusoccultus and Natrono but also they possess useful physiological monaspharaonis show protiolytic activity properties which can facilitate their with potential industrial applications. exploitation for commercial purposes. Here, we discuss some of the current industrial Amylases are used industrially in the applications of these halophiles and production of high fructose corn syrup emphasize some expected future (hydrolysis of corn starch), the textile developments. industry and are also used in laundry detergents. Halomonas meridian, Fermented Foods Haloarcula hispanica and Natronococcus amylolyticu are some of halophilic bacteria Different fermented food products are from which amylases have been prepared at a high salt concentration. For the characterized. preparation of such type of food products different microorganism are useful which Halophilc restriction endonuclease have can survive in such type of condition. For diverse application. For the industrial examplein preparation of Thai fish sauce production of the flavoring agent 5 -inosinic (nam pla) the first halophilic archaeon acid and 5 -guanylic acid Nuclease H isolated resembles Halobacterium produced by M. varians subsp. halophilus salinarum (Thongthai and Suntinanalert, is useful (Kamekura M etal., 1982). Some of 1991 and Thongthai et al., 1992) and endonucleases HacI, HcuI, HhlI and HsaI Halococcus thailandensis and Natrinema have been isolated and produced on gari , were two new species recently isolated commercial scale from Halococcus (Namwong et al.,2007 and Tapingkae et al., acetoinfaciens, Halobacterium cutirubrum, 2008). In of H. halobium and Halobacterium salinarium halophilic lactococci (Tetragenococcus respectively. halophilus) are used as starters (Kushneret al., 1998) .In the preparation of fermented Esterases and lipases are widely used as liver sauce Tetragenococcus muriatianus is biocatalysts and are also useful ingredients involved. Halalkalicoccus jeotgali is a novel in laundry detergents. The lipase from isolate obtained from shrimp jeotgal (Roh et Thermomyces lanuginosus is commercially al., 2007). produced and sold as Lipolase by Novozymes, Denmark since 1989. An Halophilic Enzymes esterase from Haloarculam arismortui has also been purified and characterized. Some of the halophilic bacteria produce hydrolytic enzymes which are stable at high Cellulase is used for commercial food salt concentration. These enzymes have processing in coffee and in textile industry, diverse application in different fields. Some laundry detergents, in pulp and paper of these enzymes are proteases which have industry and they are even used for broad application in detergents, leather pharmaceutical applications (Cavaco- Paulo, industry, food industry, pharmaceutical 1998; Tolan and Foody, 1999 and Ikeda et industry and bioremediation processes al., 2006). (Anwar and Saleemuddin, 1998 and Gupta et al., 2002). Bacteria of Halobacterium Compatible Solutes species like Haloferax mediteranei, Natrial baasiatica, Natrial bamagadii, Natrono 620 Int.J.Curr.Microbiol.App.Sci (2015) 4(12): 616-629

To adapt to the osmotic stress and to keep so forth) and for pharmaceuticals and up positive turgor pressure halophiles low cosmetics is a most encouraging field molecular weight organic compounds. Some (Galinski and Tindall, 1992 and Ventosaet compatible solutes like glycine, betaine and al., 1995).It may also enable the transfer of ectoines, may be used as stress protectants genes for salt and drought tolerance from and stabilizers of enzymes, nucleic acids, moderate halophiles to agricultural crops, membranes and whole cells. The modern such as wheat, rice and barley, enabling utilization of these compounds in enzyme them to grow in more saline soils. technology (biosensor technology, PCR, and

Table.1 Microorganisms able to Produce Hydrolytic Enzymes Isolated from Different Hypersaline Environments

Isolation Site Hydrolytic Most Abundant Isolate Affiliation References Activity Assayed Hydrolytic Activity in Amylase Amylase Salinivibrio Sánchez-Porroet Almeria, Cadiz protease Halomonas al.,(2003) and Huelva lipase Chromohalobacter (Spain) DNase Bacillus- Pullulanase Salibacillus Salinicoccus Marinococcus Saltern in Lipase Amylase Halorubrum Morenoet Huelva (Spain) protease Haloarcula al.,(2009) amylase Halobacterium nuclease Salicola Salinibacter Pseudomonas HowzSoltan Lipase Lipase Salicola Rohban et Lake (Iran) amylase Halovibrio al.,(2009) protease Halomonas xylanase Oceanobacillus DNase Thalassobacillus inulinase Halobacillus pectinase Virgibacillus cellulase Gracilibacillus pulullanase Salinicoccus Piscibacillus Deep-sea amylase Amylase Danget al.,(2009) sediments of protease Bacillus the Southern lipase Cobetia Okinawa DNase Halomonas Trough (China) Methylarcula Micrococcus Myroides Paracoccus Planococcus Pseudomonas

621

Int.J.Curr.Microbiol.App.Sci (2015) 4(12): 616-629

Psychrobacter Sporosarcina Sufflavibacter Wangia SlanicPrahova amylase Lipase ND Cojoc et salt mine gelatinase Protease al.,(2009) (Romania) lipase protease cellulase xylanase Maharlu Salt protease Not defined Bacillus Ghasemi et al., Lake (Iran) lipase Paenibacillus (2011 a,b) Halobacterium Aeromonas Staphylococcus Saline desert Amylase Not defined Bacillus Khunt et al., Indian Wild (2011) Ass Sanctuary (India) Atacama amylase DNase DNase Moreno et al., Desert (Chile) protease Bacillus (2012) lipase Halobacillus DNase Pseudomonas xylanase Halomonas pullulanase Staphylococcus Arabal soil of Protease ND Virgibacillus Jayachandra et west coast of Amylase Salinicoccus al.,(2012a, b) Karnataka Lipase gelatinase inulinase Balta Alb salt Protease Amylase ND ND Neagu et al., lake from Cellulase Esterase (2013) Romania Gelatinase Solar salterns of amylase glutaminase Halomonas Biswas and Paul Orissa and West glutaminase asparaginase Cobetia (2013) Bengal, India asparaginase lipiase Halococcus xylanase caseinase cellulose gelatinase inulinase caseinase pectinase urease lipase Salt lakes of alanine- glucosidase ND P ce il 1 et al., Romania aminopeptidase -glucosidase (2014) -glucosidase glucosidase

Degradation of Toxic Compounds 622 Int.J.Curr.Microbiol.App.Sci (2015) 4(12): 616-629

Hypersaline waters and soils are often applications in industry. Thus, Yakimov et contaminated with heavy metals or other al., (1996) recently isolated a moderate halophile which synthesizes a novel toxic compounds from different sources. glycolipid belonging to a powerful novel Hypersaline wastewaters are generated class of biosurfactants.(vi) Many moderate during the manufacture of chemicals such as halophiles produce orange or pink colonies, pesticides, pharmaceuticals and herbicides probably due to the production of and during oil and gas recovery processes. carotenoids as a protective mechanism Conventional microbiological treatment against photooxidation processes. processes do not function at high salt Carotenoids have major applications in the concentrations and therefore the use of food industry as food-coloring agents and as moderately halophilic bacteria should be additives in health food products. Therefore, considered (Orenet al. 1992,1993). investigations of the utilization of moderate halophiles as producers of carotenoids could Halophiles which are able to degrade be of great interest. hydrocarbon have been isolated from different sites like (Wardand In conclusion, comparative studies of micro Brock, 1978) and Antarctic saline lakes flora in the extreme environments results in (McMeekinet al., 1993). Treatment of better understanding of the ecosystem and hypersaline wastewaters containing phenol can benefit in designing the applications. was reported by Woolard and Irvine (1992) Hypersaline environments represent a using a biofilm of a moderately halophilic valuable source of different bioactive bacterium. H. halodurans reported to cleave compounds with great economical potential benzoate and other aromatic in industrial, agricultural, chemical, compounds.DeFranket al, (1991,1993) pharmaceuticals and biotechnological isolated halophilic bacteria, which were applications The microbial diversity can showing hydrolytic activity against several prove to be a valuable future resource in organophosphorus compounds. Halophiles various industrial and biotechnological belonging to the family Halomonadaceae processes. Such microbes can also be used have been recently isolated from highly as a source of gene(s) that can increase salt saline sites contaminated with the herbicide tolerance in different crop species through 2, 4-dichlorophenoxyacetic acid, they were genetic transformation. able to utilize chloroaromatic compounds as sources of carbon and energy. Reference

Other Applications of Halophiles Amoozegar MA, Salehghamari E, Khajeh K, Kabiri M and Naddaf S. (2008). Moderately halophilic bacteria may have Production of an extracellular various other uses in biotechnology, yet to thermohalophilic lipase from a be exploited. (i) Moderate halophiles could moderately halophilic bacterium, be used in the recovery of hypersaline waste Salinivibrio sp. strain SA-2. J. Basic brines derived from the olive oil industry Microbiol.48:160 167. and leather- or fur-curing processes. (iii) Anwar A and Saleemuddin M. (1998). They may be screened for the production of Alkaline proteases.A Review. bioactive compounds such as antibiotics. Bioresource Technol. 6: 175-183. (iv) Biological surfactants derived from moderate halophiles may have a variety of 623 Int.J.Curr.Microbiol.App.Sci (2015) 4(12): 616-629

Biswas J and Paul A K. (2013).Production of Coronado MJ, Vargas C, Hofemeister J, extracellular enzymes by halophilic Ventosa A and Nieto J. (2000). bacteria isolated from solar Production and biochemical salterns.Int. J. of App. Biol and characterization of an -amylase Pharma Technol.4 :30-36. from the moderate halophile Bolobova AV, Simankova M C and Halomonas meridian. FEMS Markovich N A. (1992). Cellulase Microbiol. Lett.183: 67 71. complex of a new halophilic Cowen L E. (2008). The evolution of fungal bacterium Halocella drug resistance: Modulating the cellulolytica.Microbiol. 61: 557 562. trajectory from genotype to Bonelo G, Ventosa A, Megias M and Ruiz- phenotype. Nat. Rev.Microbiol. Berraquero F. (1984). The sensitivity 6:187-198. of halobacteria to antibiotics. FEMS Dang H, Zhu H, Wang Jand Li T. (2009). Microbial Lett.21: 341-345. Extracellular hydrolytic enzyme Boutaiba S, Bhatnagar T, Hacene H, screening of culturable heterotrophic Mitchell D A and Baratti J C. (2006). bacteria from deep-sea sediments of Preliminary characterization of a the Southern Okinawa Trough. World lipolytic activity from an extremely J. Microbiol. Biotechnol. 25: 71-79. halophilic archaeon, Natronococcus DeFrank J J and Cheng T. (1991). sp.J. Mol. Catal. B-Enzym.41: 21 26. Purification and properties of an Cabral MMS, Cence K, Zeni J, Tsai S M, organophosphorus acid anhydrase Durrer A and Foltran LL.(2011). from a halophilic bacterial isolate. J. Carotenoids production from a newly Bacteriol.173:1938 1943. isolated Sporidiobolus pararoseus DeFrank J J, Beaudry W T, Cheng T C, strain by submerged Harvey S P, Stroup A N and fermentation. Eur Food Res Szafraniec L L. (1993). Screening of Technol.233(1):159 66. halophilic bacteria and Alteromonas Cánovas D, Vargas C, Iglesias-Guerra F, sp. for organophosphorus Csonka L, Rhodes D, Ventosa A and hydrolyzing enzyme activity. Chem. Nieto J J. (1997). Isolation and Biol. Interact. 87:141 148. characterization of salt-sensitive El-Banna AaE-R, El-Razek AM A and El- mutants of the moderate halophile Mahdy AR.(2012). Isolation, Halomonas elongata and cloning of identification and screening of the ectoine synthesis genes. J. Biol. carotenoid-producing strains of Chem.272:25794 25801. Rhodotorula glutinis. Food Nutr Cavaco-Paulo A. (1998). Mechanism of (Roma).3(5):627 33. cellulase action in textile processes. Enache M, Popescu G, Dumitru L and Carbohydr. Polym. 37: 273-277. Kamekura M. (2009). The effect of Cojoc R, Merciu S, Popescu G, Dumitru L, Na+/Mg2+ ratio on the amylase Kamekura M and Enache M. activity of haloarchaea isolated from (2009).Extracellular hydrolytic Techirghiol lake, Romania, a low salt enzymes of halophilic bacteria environment. Proc. Rom. Acad. isolated from a subterranean rock salt Series B. 11: 3 7. crystal, Rom. Biotechnol. Lett. 14: Fukushima T, Mizuki T, Echigo A, Inoue A 4658 4664. and Usami R. (2005). Organic solvent tolerance of halophilic -

624 Int.J.Curr.Microbiol.App.Sci (2015) 4(12): 616-629

amylase from a haloarchaeon, archaebacteria to antibiotics. Zbl Haloarcula sp. strain S-1. Baktl Hyg 1 Abt OrigC.2: 11-20. Extremophiles.9:85 89. Ikeda Y, Park E Y and Okida N. (2006). Galinski E A and Tindall B J. (1992). Bioconversion of waste office paper Biotechnological prospects for to gluconic acid in a turbine blade halophiles and halotolerant micro- reactor by the filamentous organisms. In: Herbert R A, Sharp R Aspergillus niger. Bioresour. J, editors. Molecular and Technol. 97: 1030-1035. biotechnology of extremophiles. Irshad A, Ahmad I and Kim S B. (2013). Glasgow, United Kingdom: Blackie. Isolation, characterization and 76 114. antimicrobial activity of halophilic Galinski EA. (1993). Compatible solutes of bacteria in foreshore soils. African J. halophilic eubacteria: Molecular Microbiol Research.7: 164-173. principles, water-solute interaction, Jayachandra S Y, Parameshwar A B, Mohan stress protection. Experientia.49:487- Reddy K and Sulochana M B. 496. (2012a).Characterization of Ghasemi Y, Rasoul-Amini S, extracellular hydrolytic enzymes Ebrahiminezhad A, Kazemi A , producing extremely Shahbazia Mand Talebniaa N. halophilicbacterium Virgibacillus sp. (2011a). Screening and Isolation of JS5.World J. of Sci. and Technol. Extracellular Protease Producing 2(2):23-26. Bacteria from the Maharloo Salt Jayachandra S Y, Anil Kumar S, Merley D P Lake. IranJ. Pharm. Sci.7:175-180. and Sulochana M B. (2012b). Ghasemi Y, Rasoul-Amini S, Kazemi A, Isolation and characterization of Zarrini G, Morowvat M T and Kargar extreme halophilic bacterium M. (2011b). Isolation and Salinicoccus sp.JAS4 producing Characterization of Some Moderately extracellular hydrolytic enzymes. Halophilic Bacteria with Lipase Recent Research in Sci. and Technol Activity. Microbiol.80, 483-487. 2012, 4(4): 46-49 Gimenez MI, Studdert CA, Sanchez J J and Jehlicka J, Edwards H G and Oren A.(2013). De Castro RE. (2000). Extracellular Bacterioruberin and salinixanthin protease of Natrialba magadii: carotenoids of extremely halophilic purification and biochemical Archaea and Bacteria: a Raman characterization.Extremophiles.4,181 spectroscopic study. Spectrochim 188. Acta. A Mol. Biomol. Good W A and Hartman P A.(1970). Spectrosc.106:99 103. Properties of the amylase from Kamekura M and Onishi H.(1974).Protease Halobacterium halobium. J. formation by a moderately Bacteriol.104:601 603. halophilic Bacillus strain.Appl. Gupta R, Beg Q K and Lorenz P. (2002). Microbiol. 27: 809 810 Bacterial alkaline proteases: Kamekura M, Hamakawa T and Onishi H. molecular approaches and industrial (1982). Application of halophilic applications. App. Microbiol and nuclease H of Micrococcus varians Biotechnol.59: 15-32. subsp. halophilus to commercial Hilpert R, Winter J, Hammes W and Kandler production of flavoring agent 5 - O. (1981). The sensitivity of

625 Int.J.Curr.Microbiol.App.Sci (2015) 4(12): 616-629

GMP. Appl. Environ. Microbiol. Lama L, Romano I,Calandrelli V,Nicolaus B 44:994 995. and Gambacorta A Kamekura M and Seno Y.(1990). A .(2005).Purification and halophilic extracellular protease from characterization of a protease a halophilic archaebacterium 172 produced by an aerobic P1.Biochem. Cell Biol. 68: 352 359. haloalkaliphilic species belonging to Kamekura M, Seno Y, Holmes M L and the Salinivibrio genus. Res. Dyall-Smith M L. (1992). Molecular Microbiol. 156:S478 484 cloning and sequencing of the gene Li Z, Sun M, Li Q, Li A and Zhang C. for a halophilic alkaline serine (2012). Profiling of carotenoids in six protease (halolysin) from an microalgae (Eustigmatophyceae) and unidentified halophilic archaea strain assessment of their beta-carotene (172P1) and expression of the gene productions in bubble column in Haloferax volcanii.J. Bacteriol. photobioreactor. Biotechnol. 174: 736 742. Lett.34(11):2049 53 Kamekura M, Seno Y and Dyall-Smith ML. MacElroy R D.(1974).Some comments on (1996). Halolysin R4, a serine evolution of Extremophiles. proteinase from the halophilic Biosystems.6: 75-75 archaeon Haloferax mediterranei; Madigan M T and Oren A. (1999). gene cloning, expression and Thermophilic and halophilic structural studies. Biochim. Biophys. extremophiles. Curr. Opin. Acta.1294:159 167. Microbiol.2:265 269. Khunt M, Pandhi N and Rana A. (2011). Margesin R and Schinner F. (2001). Potential Amylase from moderate halophiles of halotolerant and halophilic isolated from wild ass excreta. Int. J. microorganisms for biotechnology. Pharm. Bio. Sci. 1: 586-592. Extremophiles.5:73 83. Kobayashi T, Kamekura M, Kanlayakrit W McMeekin T A, Nichols P D, Nichols S D, and Onishi H. (1986). Production, Juhasz A and Franzmann P D. purification, and characterization of (1993). Biology and biotechnological an amylase from the moderate potential of halotolerant bacteria halophile, Micrococcus varians from Antarctic saline lakes. subsp. halophilus. Microbios Experientia.49:1042 1046. .46:165 177. Moreno M L, García M T, Ventosa A and Kobayashi T, Kamai H, Aono R, Horikoshi Mellado E. (2009). Characterization K and Kudo T. (1992). of Salicola sp. IC10, a lipase- and Haloalkaliphilic maltotriose-forming protease-producing extreme -amylase from the archaebacterium halophile. FEMS Microbiol. Ecol.68: Natronococcus sp. strain Ah-36. J. 59-71. Bacteriol.174: 3439 3444. Moreno M L, Piubeli F, Bonfá M R, García Kumar C G, Joo H S, Koo Y M, Paik S R M T , Durrant L Rand Mellado E. and. Chang C S.(2004). (2012). Analysis and characterization Thermostable alkaline protease from of cultivable extremophilic a novel marine hydrolytic bacterial community in haloalkalophilic Bacillus heavy-metal-contaminated soils from clausii isolate. World J. Microbiol. the Atacama Desert and their Biotechnol.20: 351 357.

626 Int.J.Curr.Microbiol.App.Sci (2015) 4(12): 616-629

biotechnological potentials. J. Appl. aspects of halophilic Microbiol.113: 550-559. microorganisms. New York, N.Y: Namwong S, Tanasupawat S, Visessanguan Plenum Press. 341 349. W, Kudo T and Itoh T. Oren A, Gurevich P, Azachi M and Henis Y. (2007).Halococcus thailandensissp. (1992). Microbial degradation of nov., from fish sauce in Thailand. Int. pollutants at high salt concentrations. J. Syst. Evol. Microbiol. 57: 2199 Biodegradation.3:387 398. 2203. Oren A, Gurevich P, Azachi M and Henis Y. Naziri D, Hamidi M, Hassanzadeh S, Tarhriz (1993). Microbial degradation of V, Zanjani B M, Nazemyieh H, pollutants at high salt concentrations. Hejazi M A and Hejazi M S.(2014). In: Rosenberg E, editor. Analysis of Carotenoid Production Microorganisms to combat pollution. by Halorubrum sp. TBZ126; an Dordrecht, The Netherlands: Kluwer Extremely Halophilic Archeon from Academic Publishers. 263 274. Urmia Lake. Adv. Pharma. Bull. Oren A. (2008). Microbial life at high salt 4(1): 61-67. concentrations: phylogenetic and Neagu S, Enache M and Cojoc R. (2013). metabolic diversity.Saline Systems. Extracellular hydrolytic activities of Oren A.(2010). Industrial and environmental halophilic microorganisms isolated applications of halophilic from Balta Alb salt lake. Romanian microorganisms. Environ. Technol. Biotechnol. Letters. 19:8951-8958. 3(1): 825-834. Norberg P and Hofsten B.(1969). Proteolytic Ozcan B, Ozyilmaz G, Cokmus C and enzymes from extremely halophilic Caliskan M.(2009). Characterization bacteria. J. Gen. Microbiol. 55: 251 of extracellular esterase and lipase 256. activities from five halophilic Onishi H, Fuchi H, Konomi K, Hidaka O and archaeal strains. J. Ind. Microbiol. Kamekura M. (1980). Isolation and Biotechnol.36:105 110. distribution of a variety of halophilic P ce il 1 I, Cojoc R and Enache1 M.(2014). bacteria and their classification by Evaluation of halobacterial salt-response. Agric. Biol. extracellular hydrolytic activities in Chem.44:1253 1258. several natural saline and hypersaline Onishi H, Mori T, Takeuchi S, Tani K, lakes from Romania. British Kobayashi T and Kamekura M. Biotechnol J. 4(5): 541-550. (1983). Halophilic nuclease of a Patel S, Jain N and Madamwar D. (1993). moderately halophilic Bacillus sp.: Production of -amylase from production, purification and Halobacterium halobium.World J. characteristics. Appl. Environ. Microbiol. Biotechnol.9:25 28. Microbiol.45:24 30. Pearson and Carol. (2008). Antibiotic Onishi H, Yokoi H and Kamekura M. resistance fast-growing problem (1991).An application of a bioreactor worldwide. Voice of America. 12-29. with flocculated cells of halophilic Perez-Pomares F, Bautista V, Ferrer J, Pire Micrococcus varians subsp. C, Marhuenda-Egea F C and Bonete halophilus which preferentially MJ. (2003). -Amylase activity from adsorbed halophilic nuclease H to 5 - the halophilic archaeon Haloferax nucleotide production. In: Rodriguez- mediterranei. Extremophiles. 7:299 Valera F, editor. General and applied 306.

627 Int.J.Curr.Microbiol.App.Sci (2015) 4(12): 616-629

Rani M H S, Ramesh T, Subramanian J and like enzyme from the archaeon Kalaiselvam M. (2013). Production Natronomonas pharaonis and other and Characterization of Melanin halobacteria.Extremophiles.3: 153 Pigment from Halophilic Black 161. YeastHortaea werneckii. Int. J. of Stepanov V M, Rudenskaya G N, Revina L Pharma. Res. & Review. 2(8):9-17. P, Gryaznova Y B, Lysogorskaya E Roh S W, Nam Y D, Chang H W, Sung Y, N, Filippova I Y, Ivanova I I. (1992). Kim K H, Oh H M and Bae J A serine proteinase of an W.(2007). Halalkalicoccus jeotgali archaebacterium Halobacterium sp. nov., a halophilic archaeon from mediterranei homologue of shrimp jeotgal, a traditional Korean eubacterial subtilisins. Biochem. J. fermented seafood,Int. J. Syst. Evol. 285: 281 286. Microbiol. 57: 2296 2298. Studdert CA, De Castro RE, Seitz K H and Rohban R, Amoozegar M A and Ventosa A. Sanchez J J.(1997).Detection and (2009). Screening and isolation of preliminary characterization of halophilic bacteria producing extracellular proteolytic activities of extracellular hydrolysis from Howz the haloalkaliphilic archaeon Soltan Lake, Iran. J. Ind. Microbiol. Natronococcus occultus. Arch. Biotechnol.36: 333-340. Microbiol.168: 532 535. Ryu K, Kim J and Dordick JS. (1994). Tapingkae W, Tanasupawat S, Itoh T, Parkin Catalytic properties and potential of KL, Benjakul S, Visessanguan W an extracellular protease from an and Valyasevi R. (2008). Natrinema extreme halophile.Enzyme Microbiol. gari sp. nov., a halophilic archaeon Technol. 16: 266 275. isolated from fish sauce in Sánchez-Porro C, Martín S, Mellado E and Thailand.Int. J. Syst. Evol. Ventosa A. (2003). Diversity of Microbiol. 58: 2378 2383. moderately halophilic bacteria Thongthai C and Suntinanalert P. (1991). producing extracellular hydrolytic Halophiles in Thai fish sauce (nam enzymes. J. Appl. Microbiol. 94: pla) In: Rodriguez-Valera F, editor. 295-300. General and applied aspects of Sawale A, Kadam T A, Karale M A and halophilic microorganisms. New Kadam O A. (2014).Antimicrobial York, N.Y: Plenum Press.381 388. Activity of Secondary Metabolites Thongthai C, McGenity T J, Suntinanalert P from Halophilic Bacillus pumilus and Grant W D. (1992). Isolation and sp.Int.J.Curr.Microbiol.Appl.Sci. 3: characterization of an extremely 506-512. halophilic archaeobacterium from Singh SK, Tripathi VR, Jain RK, Vikram S traditionally fermented Thai fish and Garg SK. (2010). An antibiotic, sauce (nam pla).Lett. Appl. heavy metal resistant and Microbiol. 14: 111 114. halotolerant Bacillus cereus SIU1 Todkar S, Todkar R, Kowale L, Karmarkar and its thermoalkaline protease. K and Kulkarni A. (2012). Isolation Microb Cell Fact. 10.1186/1475- and Screening of Antibiotic 2859-9-59 . producing Halophiles from Ratnagri Stan-Lotter H, Doppler E, Jarosch M, Radax coastal area, State of Maharahstra. C, Gruber C and Inatomi K. (1999). International Journal of Scientific Isolation of a chymotrypsinogen B

628

Int.J.Curr.Microbiol.App.Sci (2015) 4(12): 616-629

and Research Publications. 2:2250- 3153. Tolan J S and Foody B. (1999). Cellulase from submerged fermentation. In:Tsao GT (ed.). Recent Progress in Bioconversion of Lignocellulosics.Springer-Verlag, Berlin. Adv. Biochem. Eng. Biotechnol. 41-67. Ventosa A and Nieto J J. (1995). Biotechnological applications and potentialities of halophilic microorganisms.World J. Microbiol. Biotechnol.11:85 94. Vreeland R H, Piselli Jr A F, McDonnough S and Meyers S S.(1998).Distribution and diversity of halophilic bacteria in a subsurface salt formation.Extremophiles.2: 321 331. Ward D M and Brock T D. (1978). Hydrocarbon biodegradation in hypersaline environments. Appl. Environ. Microbiol.35:353 359. Woolard C R and Irvine R L. (1992). Abstracts of the Annual Water Environmental Federation Conference. Biological treatment of hypersaline wastewater by a biofilm of halophilic bacteria. Abstr. 14. Yakimov M M, Golyshin P N, Lang S, Wagner F, Moore E, Abraham W R and Timmis K N. (1996). Abstracts of the First International Congress on Extremophiles.New moderate halophilic marine strain MM1 produces novel class of biosurfactants. Abstr. 182.

629