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Exploring the multiple biotechnological potential of halophilic microorganisms isolated from two Argentinean salterns

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Abstract

The biodiversity and biotechnological potential of microbes from central Argentinean halophilic environments have been poorly explored. Salitral Negro and Colorada Grande salterns are neutral hypersaline basins exploded for NaCl extraction. As part of an ecological analysis of these environments, two bacterial and seven archaeal representatives were isolated, identified and examined for their biotechnological potential. The presence of hydrolases (proteases, amylases, lipases, cellulases and nucleases) and bioactive molecules (surfactants and antimicrobial compounds) was screened. While all the isolates exhibited at least one of the tested activities or biocompounds, the species belonging to Haloarcula genus were the most active, also producing antimicrobial compounds against their counterparts. In general, the biosurfactants were more effective against olive oil and aromatic compounds than detergents (SDS or Triton X-100). Our results demonstrate the broad spectrum of activities with biotechnological potential exhibited by the microorganisms inhabiting the Argentinean salterns and reinforce the importance of screening pristine extreme environments to discover interesting/novel bioactive molecules.

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References

  • Albarracín VH, Pathak GP, Douki T, Cadet J, Borsarelli CD, Gärtner W, Farias ME (2012) Extremophilic Acinetobacter strains from high-altitude lakes in Argentinean Puna: remarkable UV-B resistance and efficient DNA damage repair. Orig Life Evol Biosph 42:201–221

    Article  PubMed  Google Scholar 

  • Antón J, Oren A, Benlloch S, Rodriguez-Valera F, Amann R, Rossello-Mora R (2002) Salinibacter ruber gen nov., sp nov., a novel, extremely halophilic member of the bacteria from saltern crystallizer ponds. Int J Syst Evol Microbiol 52:485–491

    Article  CAS  PubMed  Google Scholar 

  • Atanasova NS, Pietila MK, Oksanen HM (2013) Diverse antimicrobial interactions of halophilic archaea and bacteria extend over geographical distances and cross the domain barrier. Microbiology Open 2:811–825

    PubMed Central  PubMed  Google Scholar 

  • Belfiore C, Ordóñez OF, Farías ME (2013) Proteomic approach of adaptive response to arsenic stress in Exiguobacterium sp. S17, an extremophile strain isolated from a high-altitude Andean Lake stromatolite. Extremophiles 17:421–431

    Article  CAS  PubMed  Google Scholar 

  • Benlloch S, López-López A, Casamayor E, Øvreås L, Goddard V, Daae FL, Smerdon G, Massana R, Joint I, Thingstad F, Pedrós-Alió C, Rodríguez-Valera F (2002) Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ Microbiol 4:349–360

    Article  PubMed  Google Scholar 

  • Bhatnagar T, Boutaiba S, Hacene H, Cayol J-L, Fardeau M-L, Ollivier B, Baratti J (2005) Lipolytic activity from Halobacteria: screening and hydrolase production. FEMS Microbiol Lett 248:133–140

    Article  CAS  PubMed  Google Scholar 

  • Birbir M, CalliB MB, 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 23:309–316

    Article  CAS  Google Scholar 

  • Borsodi AK, Felföldi T, Máthé I, BognárV KM, Krett G, Jurecska L, Tóth EM, Márialigeti K (2013) Phylogenetic diversity of bacterial and archaeal communities inhabiting the saline Lake Red located in Sovata, Romania. Extremophiles 17:87–98

    Article  PubMed  Google Scholar 

  • Brányiková I, Maršálková B, Doucha J, Brányik T, Bišová K, Zachleder V, Vítová M (2011) Microalgae—Novel highly efficient starch producers. Biotechnol Bioeng 108:766–776

    Article  PubMed  Google Scholar 

  • Calvo C, Martinez-Checa F, Toledo FL, Porcel J, Quesada E (2002) Characteristics of bioemulsifiers synthesised in crude oil media by Halomona eurihalina and their effectiveness in the isolation of bacteria able to grow in the presence of hydrocarbons. Appl Microbiol Biotechnol 60:347–351

    Article  CAS  PubMed  Google Scholar 

  • Camacho RM, Mateos JC, Gonzalez-Reynoso O, Prado LA, Cordova J (2009) Production and characterization of esterase and lipase from Haloarcula marismortui. Ind Microbiol Biotechnol 36:901–909

    Article  CAS  Google Scholar 

  • Cameotra SS, Makkar RS (1998) Synthesis of biosurfactants in extreme conditions. Appl Microbiol Biotechnol 50:520–529

    Article  CAS  PubMed  Google Scholar 

  • Cherry JR, Fidantsef AL (2003) Direct evolution of industrial enzymes: an update. Curr Opin Biotechnol 14:438–443

    Article  CAS  PubMed  Google Scholar 

  • Cojoc R, Mercius S, Popescu G, Dumitru L, Kamekura M, Enache M (2009) Extracellular hydrolytic enzymes of halophilic bacteria isolated from a subterranean rock salt cristal. Rom Biotechnol Lett 14:4658–4664

    Google Scholar 

  • Cooper DG, Goldenberg BG (1987) Surface active agents from two Bacillus species. Appl Environ Microbiol 53:224–229

    PubMed Central  CAS  PubMed  Google Scholar 

  • De Castro RE, Maupin-Furlow JA, Giménez MI, Herrera Seitz MK, Sánchez JJ (2006) Haloarchaeal proteases and proteolytic systems. FEMS Microbiol Rev 30:17–35

    Article  PubMed  Google Scholar 

  • Delgado-Garcia M, Valdivia-Urdiales B, Aguilar-Gonzalez C, Contreras-Esquivel J, Rodriguez-Herrera R (2012) Halophilic hydrolases as a new tool for the biotechnological industries. J Sci Food Agric

  • DeLong E (1992) Archaea in costal marine environments. Proc Natl Acad Sci USA 89:5685–5689

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Djeridi I, Militon C, Grossi V, Cuny P (2013) Evidence from surfactant production by the haloarchaeon Haloferax sp. MSNC14 in hydrocarbon-containing media. Extremophile 17:669–675

    Article  CAS  Google Scholar 

  • Donio MBS, Ronica FA, Viji VT, Velmurugan S, Jenifer JSCA, Michaelbabu M, Dhar P, Citarasu T (2013) Halomonas sp. BS4, A biosurfactant producing halophilic bacterium isolated from solar salt works in India and their biomedical importance. SpringerPlus 2:149–159

    Article  PubMed Central  PubMed  Google Scholar 

  • Enache M, Kamekura M (2010) Hydrolytic enzymes of halophilic microorganisms and their ecomonic values. Rom J Biochem 47:47–59

    CAS  Google Scholar 

  • Fathepure BZ (2014) Recent studies in microbial degradation of petroleum hydrocarbons in hypersaline environments. Front Microbiol 5:173

    Article  PubMed Central  PubMed  Google Scholar 

  • Flores M, Zavaleta A, Zambrano Y, Cervantes L, Izaguirre V (2010) Bacterias halófilas moderadas productoras de hidrolasas de interés biotecnológico. Cien e Invest 13:42–46

    Google Scholar 

  • Fuciños P, Gonzalez R, Atanes E, Ferdandez Sestelo AB, Perez-Guerra N, Pastrana L, Rua ML (2012) Lipases and Esterases from Extremophiles: Overview and case example of the production and purification of an esterase from Thermus thermophilus HB27. In: Georgina S (ed) Lipases and phospholipases: methods and protocols, methods in molecular biology, vol 861. Springer, New York, pp 239–266

    Chapter  Google Scholar 

  • Gohel HR, Contractor CN, Ghosh SK, Braganza VJ (2014) A comparative study of various staining techniques for determination of extra cellular cellulase activity on Carboxy Methyl Cellulose (CMC) agar plates. Int J Curr Microbiol App Sci 3:261–266

    CAS  Google Scholar 

  • González C, Gutiérrez C, Ramírez C (1978) Halobacteriumvallismortis sp. nov. An amylolytic and carbohydrate-metabolizing, extremely halophilic bacterium. Can J Microbiol 24:710–715

    Article  PubMed  Google Scholar 

  • Hasan F, Shah AA, Hameed A (2006) Industrial applications of microbial lipases. Enzyme Microbial Technol 39:235–251

    Article  CAS  Google Scholar 

  • Ihara K, Watanabe S, Tamura T (1997) Haloarcula argentinensis sp. nov. and Haloarcula mukohataei sp. nov., two new extremely halophilic archaea collected in Argentina. Int J Syst Bacteriol 47:73–77

    Article  CAS  PubMed  Google Scholar 

  • Imadalou-Idres N, Carre-Mlouka A, Vandervennet M, Yahiaoui H, Peduzzi J, Rebuffat S (2013) Diversity and antimicrobial activity of cultivable halophilic archaea from three Algerian sites. J Life Sci 7:1057–1069

    CAS  Google Scholar 

  • Kavitha P, Lipton AP, Sarika AR, Aishwayra MS (2011) Growth characteristics and halocin production by a new isolated, Haloferax volcanii KPS1 from Kovalam solar saltern (India). Res J Biol Sci 6:257–262

    Google Scholar 

  • Kebbouche-Gana S, Gana ML, Khemili S, Fazouane-Naimi F, Bouanane NA, Penninckx M, Hacene H (2009) Isolation and characterization of halophilic Archaea able to produce biosurfactants. J Ind Microbiol Biotechnol 36:727–738

    Article  CAS  PubMed  Google Scholar 

  • Kebbouche-Gana S, Gana ML, Ferriounr I, Khemili S, Lenchi N, Aknmouci-Toumi S, Bouanane-Darefed NA, Djelali N-E (2013) Production of biosurfactant on crude date syrup under saline conditions by entrapped cells of Natrialba sp. strain E21, an extremely halophilic bacterium isolated from a solar saltern (Ain Salah, Algeria). Extremophile 17:981–993

    Article  CAS  Google Scholar 

  • Lane DJ, Pace B, Olsen GJ, Stahl D, Sogin M, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci USA 82:6955–6959

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lequerica JL, O’Connor JE, Such L, Alberola A, Meseguer I, Dolz M, Torreblanca M, Moya A, Colom F, Soria B (2006) A halocin acting on Na+/H+ exchanger of Haloarchaea as a new type of inhibitor in NHE of mammals. J Physiol Biochem 62:253–262

    Article  CAS  PubMed  Google Scholar 

  • Li W, Yu H-Y (2013) Halostable cellulose with organic solvent tolerance from Haloarcula sp LLSG7 and its application in bioethanol fermentation using agricultural wastes. J Ind Microbiol Biotechnol 40:1357–1365

    Article  CAS  PubMed  Google Scholar 

  • Litchfield CD (2011) Potential for industrial products from halophilic Archaea. J Int Microbiol Biotechnol 38:1635–1647

    Article  CAS  Google Scholar 

  • Lizama C, Monteoliva-Sanchez M, Suarez-Garcia A, Rosello-Mora R, Aguilera M, Campos V, Ramos-Cormenzana A (2002) Halorubrum tebenquichense sp. nov., a novel halophilic archaeon isolated from Atacama saltern. Chile. Int J Syst Evol Microbiol 52:149–155

    Article  CAS  PubMed  Google Scholar 

  • Llamas I, Amjres H, Mata JA, Quesada E, Béjar V (2012) The potential biotechnological applications of the exopolysaccharide produced by the halophilic bacterium Halomonas almeriensis. Molecules 17:7103–7120

    Article  CAS  PubMed  Google Scholar 

  • Madern D, Ebel C, Zaccai G (2000) Halophilic adaptations of enzyme. Extremophile 4:91–98

    Article  CAS  Google Scholar 

  • Margesin R, Schinner F (2001) Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 5:73–83

    Article  CAS  PubMed  Google Scholar 

  • Marhuenda-Egea FC, Bonete MJ (2002) Extreme halophilic enzymes in organic solvents. Curr Opin Biotechnol 13:385–389

    Article  CAS  PubMed  Google Scholar 

  • Maturrano L, Valens-Vadell M, Rosello-Mora R, Antón J (2006) Salicola marasensis gen. nov., sp. nov., an extremely halophilic bacterium isolated from the Maras solar salterns in Peru. Int J Syst Evol Microbiol 56:1685–1691

    Article  CAS  PubMed  Google Scholar 

  • Meseguer I, Rodríguez Valera F (1985) Production and purification of halocin H4. FEMS Microbiol Lett 28:177–182

    Article  CAS  Google Scholar 

  • Moreno ML, García MT, Ventosa A, Mellado E (2009) Characterization of Salicola sp. IC10, a lipase and protease producing extreme halophile. FEMS Microbiol Ecol 68:59–71

    Article  Google Scholar 

  • Moreno ML, Pérez D, García MT, Mellado E (2013) Halophilic bacteria as a source of novel hydrolytic enzymes. Life 3:38–51

    Article  CAS  Google Scholar 

  • Mutlu MB, Martínez-García M, Santos F, Peña A, Guven K, Antón J (2008) Prokaryotic diversity in Tuz Lake, a hypersaline environment in Inland Turkey. FEMS Microbiol Ecol 65:474–483

    Article  CAS  PubMed  Google Scholar 

  • Nguyen TH, Vu VH (2012) Bioethanol production from marine algae biomass: prospect and troubles. J Viet Env 3:25–29

    Google Scholar 

  • O’Connor EM, Shand RF (2002) Halocins and sulfolobicins: the emerging story of archaeal protein and peptide antibiotics. J Ind Microbiol Biotech 28:23–31

    Article  Google Scholar 

  • Ochsenreiter T, Pfeifer F, Schleper C (2002) Diversity of Archaea in hypersaline environments characterized by molecular-phylogenetic and cultivation studies. Extremophiles 6:267–274

    Article  CAS  PubMed  Google Scholar 

  • Oren A (2010) Industrial and environmental applications of halophilic microorganisms. Environ Technol 31:825–834

    Article  CAS  PubMed  Google Scholar 

  • Ozcan B, Ozyilmaz G, Cokmus C, Caliskan M (2009) Characterization of extracellular esterase and lipase activities from five halophilic archaeal strains. J Ind Microbiol Biotechnol 36:105–110

    Article  CAS  PubMed  Google Scholar 

  • Peat S, Turvey JR (1965) Polysaccharides of marine algae. In: Zechmeister L (ed) Progress in the chemistry of organic natural products. Springer, Vienna, pp 1–45

    Google Scholar 

  • Plou F, Ferrer M, Nuero O, Calvo M, Alcalde M, Reyes F, Ballesteros A (1998) Analysis of Tween 80 as an esterase/lipase substrate for lipolytic activity assay. Biotechnol Technol 12:183–186

    Article  CAS  Google Scholar 

  • Price L, Shand R (2000) Halocin S8: a 36-amino-acid microhalocin from the haloarchaeal strain S8a. J Bacteriol 182:4951–4958

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reis RS, Pacheco GJ, Pereira AG, Freire DMG (2013) Biosurfactants: Production and Applications. In: Chamy R, Rosenkranz F (eds,) Biodegradation: life of science, ISBN 978-953-51-1154-2, InTech. Doi: 10.5772/56144

  • Richard SB, Madern D, Garcin E, Zaccai G (2000) Halophilic adaptation: novel solvent protein interactions observed in the 2.9 and 2.6 A resolution structures of the wild type and a mutant of malate dehydrogenase from Haloracula marismortui. Biochem 39:992–1000

    Article  CAS  Google Scholar 

  • Ruiz DM, Iannuci NB, Cascone O, De Castro RE (2010) Peptide synthesis catalysed by a haloakaliphilic serine protease from the archaeon Natrialba magadii (Nep). Lett Appl Microbiol 51:691–696

    Article  CAS  PubMed  Google Scholar 

  • Sabet S, Diallo L, Hays L, Jung W, Dillon JG (2009) Characterization of halophiles isolated from solar salterns in Baja California, Mexico. Extremophiles 13:643–656

    Article  PubMed  Google Scholar 

  • Sarafin Y, Donio MBS, Velmurugan S, MichaelbabuM CT (2014) Kocuria marina BS-15 a biosurfactant producing halophilic bacteria isolated from solar salt works. Saudi J Biol Sci Ind. doi:10.1016/j.sjbs.2014.01.001

    Google Scholar 

  • Satpute SK, Banat I, Dhakephalkar PK, Banpurkar AG, Chopade BA (2010) Biosurfactants, bioemulsifiers and exopolysaccharides from marine microorganisms. Biotechnol Adv 28:436–450

    Article  CAS  PubMed  Google Scholar 

  • Selim SA, El-Alfy SM, Hagagy NI, Hassanin AAI, Khattab RM, El-Meleigy ESAA, Aziz MHA, Maugeri TL (2012) Oil-biodegradation and biosurfactant production by haloalkaliphilic archaea isolated from soda lakes of the Wadi An Natrun, Egypt. J Pure Appl Microbiol 6:1011–1020

    CAS  Google Scholar 

  • Singh A, van Hamme JD, Ward OP (2007) Surfactants in microbiology and biotechnology: part 2. Application aspects. Biotechnol Adv 25:99–121

    Article  CAS  PubMed  Google Scholar 

  • Takashina T, Hamamoto T, Otozai K, Grant WD, Horikoshi K (1990) Haloarcula japonica sp.nov., a new triangular halophilic archaebacterium. Syst Appl Microbiol 13:177–181

    Article  CAS  Google Scholar 

  • Tirunarayanan MO, Lundbeck H (1968) Investigations on the enzymes and toxins of staphylococci. Acta Pathol Microbiol Scand 72:263–276

    Article  CAS  PubMed  Google Scholar 

  • Torreblanca M, Meseguer I, Ventosa A (1994) Production of halocin is a practically universal feature of archaeal halophilic rods. Lett Appl Microbiol 19:201–205

    Article  CAS  Google Scholar 

  • van Hamme JD, Singh A, Ward OP (2006) Physiological aspects. Part 1 in a series of papers devoted to surfactants in microbiology and biotechnology. Biotechnol Adv 24:604–620

    Article  PubMed  Google Scholar 

  • Venkatachalam S, Sivaprakash M, Gowdaman V, Prabagaran S (2014) Bioprospecting of cellulase producing extremophilic bacterial isolates from India. Br Microbiol Res J 4:142–154

    Article  Google Scholar 

  • Ventosa A, Sanchez-Porro S, Mellado E et al (2005) Halophilic archaea and bacteria as a source of extracellular hydrolytic enzymes. In: Gunde-Cimerman N (eds) Adaptation to life at high salt concentration in Archaea, Bacteria, and Eukarya, Springer, pp 337–354

  • Wu L, Yao J, Jain AK, Chandankere R, Duan X, Richnow HH (2014) An efficient thermotolerant and halophilic biosurfactant-producing bacterium isolated from Dagang oil field for MEOR application. Int J Curr Microbiol Appl Sci 3:586–599

    CAS  Google Scholar 

  • Yachai M, Tanasupawat S, Itoh T, Benjakul S, Visessanguan W, Valyasevi R (2008) Halobacterium piscisalsi sp. nov., from fermented fish (pla-ra) in Thailand. Int J Syst Evol Microbiol 58:2136–2140

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants from Agencia Nacional de Promoción Científica y Técnica [ANPCyT, PICT 1247/10], Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, PIP 1783 and 1106), and Universidad Nacional de Mar del Plata (UNMdP), Argentina.

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  1. Instituto de Investigaciones Biológicas, CONICET-Universidad Nacional de Mar del Plata, Funes 3250 4to Nivel, 7600, Mar del Plata, Argentina

    Débora Nercessian, Leonardo Di Meglio, Rosana De Castro & Roberto Paggi

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  1. Débora Nercessian
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  2. Leonardo Di Meglio
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  3. Rosana De Castro
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  4. Roberto Paggi
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Correspondence to Débora Nercessian or Roberto Paggi.

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Communicated by M. da Costa.

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Nercessian, D., Di Meglio, L., De Castro, R. et al. Exploring the multiple biotechnological potential of halophilic microorganisms isolated from two Argentinean salterns. Extremophiles 19, 1133–1143 (2015). https://doi.org/10.1007/s00792-015-0785-7

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