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Production and properties of an exopolysaccharide synthesized by the extreme halophilic archaeon Haloterrigena turkmenica

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Abstract

We have isolated a novel exopolysaccharide (EPS) produced by the extreme halophilic archaeon Haloterrigena turkmenica. Some features, remarkable from an industrial point of view, such as emulsifying and antioxidant properties, were investigated. H. turkmenica excreted 20.68 mg of EPS per 100 ml of culture medium when grown in usual medium supplemented with glucose. The microorganism excreted the biopolymer mainly in the middle exponential growth phase and reached the maximal production in the stationary phase. Analyses by anion exchange chromatography and SEC-TDA Viscotek indicated that the EPS was composed of two main fractions of 801.7 and 206.0 kDa. It was a sulfated heteropolysaccharide containing glucose, galactose, glucosamine, galactosamine, and glucuronic acid. Studies performed utilizing the mixture of EPS anionic fractions showed that the biopolymer had emulsifying activity towards vegetable oils comparable or superior to that exhibited by the controls, moderate antioxidant power when tested with 2,2′-diphenyl-1-picrylhydrazyl (DPPH·), and moisture-retention ability higher than hyaluronic acid (HA). The EPS from H. turkmenica is the first exopolysaccharide produced by an archaea to be characterized in terms of properties that can have potential biotechnological applications.

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References

  • Allison DG, Sutherland IW (1984) A staining technique for attached bacteria and its correlation to extracellular carbohydrate production. J Microbiol Meth 2(2):93–99

    Article  CAS  Google Scholar 

  • Amouric A, Liebgott PP, Joseph M, Brochier-Armanet C, Lorquin J (2014) Halomonas olivaria sp. nov., a moderately halophilic bacterium isolated from olive-processing effluents. Int J Syst Evol Microbiol 64(1):46–54

    Article  PubMed  CAS  Google Scholar 

  • Antón J, Meseguer I, Rodríguez-Valera F (1988) Production of an extracellular polysaccharide by Haloferax mediterranei. Appl Environ Microbiol 54(10):2381–2386

    PubMed  PubMed Central  Google Scholar 

  • Arena A, Maugeri TL, Pavone B, Jannello D, Gugliandolo C, Bisignano G (2006) Antiviral and immunoregulatory effect of a novel exopolysaccharide from a marine thermotolerant Bacillus licheniformis. Int Immunopharmacol 6(1):8–13

    Article  PubMed  CAS  Google Scholar 

  • Arena A, Gugliandolo C, Stassi G, Pavone B, Iannello D, Bisignano G, Maugeri TL (2009) An exopolysaccharide produced by Geobacillus thermodenitrificans strain B3-72: antiviral activity on immunocompetent cells. Immunol Lett 123(2):132–137

    Article  PubMed  CAS  Google Scholar 

  • Arias S, Ferrer MR, Del Moral A, Quesada E, Béjar V (2003) Mauran, an exopolysaccharide produced by the halophilic bacterium Halomonas maura, with a novel composition and interesting properties for biotechnology. Extremophiles 7(4):319–324

    Article  PubMed  CAS  Google Scholar 

  • Augustine R, Rajendran R, Cvelbar U, Mozetič M, George A (2013) Biopolymers for health, food, and cosmetic applications. In: Thomas S, Durand D, Chassenieux C, Jyotishkumar P (eds) Handbook of biopolymer-based materials: from blends and composites to gels and complex networks. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, pp 801–849

    Chapter  Google Scholar 

  • Becker A, Katzen F, Pühler A, Ielpi L (1998) Xanthan gum biosynthesis and application: a biochemical/genetic perspective. Appl Microbiol Biotechnol 50(2):145–152

    Article  PubMed  CAS  Google Scholar 

  • Béjar V, Llamas I, Calvo C, Quesada E (1998) Characterization of exopolysaccharides produced by 19 halophilic strains included in the species Halomonas eurihalina. J Biotechnol 61(2):135–141

    Article  Google Scholar 

  • Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239(1):70–76

    Article  PubMed  CAS  Google Scholar 

  • Bhaskar PV, Bhosle NB (2005) Microbial extracellular polymeric substances in marine biogeochemical processes. Curr Sci 88(1):45–53

    CAS  Google Scholar 

  • Blois MS (1958) Antioxidant determination by the use of a stable free radical. Nature 181(4617):1199–1200

    Article  CAS  Google Scholar 

  • Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Chem 54(2):484–489

    CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72(1–2):248–254

    Article  PubMed  CAS  Google Scholar 

  • Cerning J, Renard CMGC, Thibault JF, Bouillanne C, Landon M, Desmazeaud M, Topisirovic L (1994) Carbon source requirements for exopolysaccharide production by Lactobacillus casei CG11 and partial structure analysis of the polymer. Appl Environ Microbiol 60(11):3914–3919

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chen L, Du Y, Zeng X (2003) Relationships between the molecular structure and moisture-absorption and moisture-retention abilities of carboxymethyl chitosan. II. Effect of degree of deacetylation and carboxymethylation. Carbohydr Res 338(4):333–340

    Article  PubMed  CAS  Google Scholar 

  • Cojoc R, Merciu S, Oancea P, Pincu E, Dumitru L, Enache M (2009) Highly thermostable exopolysaccharide produced by the moderately halophilic bacterium isolated from a man-made young salt lake in Romania. Pol J Microbiol 58(4):289–294

    PubMed  CAS  Google Scholar 

  • Cooper DG, Goldenberg BG (1987) Surface active agents of two Bacillus species. Appl Environ Microbiol 53(2):224–229

    PubMed  PubMed Central  CAS  Google Scholar 

  • Duboc P, Mollet B (2001) Applications of exopolysaccharides in dairy industry. Int Dairy J 11(9):759–768

    Article  CAS  Google Scholar 

  • Dubois MK, Gilles A, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric methods for determination of sugars of related substances. Anal Chem 28(3):350–356

    Article  CAS  Google Scholar 

  • Fang CJ, Ku KL, Lee MH, Su NW (2010) Influence of nutritive factors on C50 carotenoids production by Haloferax mediterranei ATCC 33500 with two-stage cultivation. Bioresour Technol 101(16):6487–6493

    Article  PubMed  CAS  Google Scholar 

  • Freitas F, Alves VD, Reis MA (2011) Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends Biotechnol 29(8):388–398

    Article  PubMed  CAS  Google Scholar 

  • Gorret AU, Maubois N, Engasser JL, Ghoul JM (2001) Study of the effects of temperature, pH and yeast extract on growth and exopolysaccharide production by Propionibacterium acidi-propionici on milk microfiltrate using a response surface methodology. J Appl Microbiol 90(5):788–796

    Article  PubMed  CAS  Google Scholar 

  • Guo S, Mao W, Han Y, Zhang X, Yang C, Chen Y, Xu J, Li H, Qi X (2010) Structural characteristics and antioxidant activities of the extracellular polysaccharides produced by marine bacterium Edwardsiella tarda. Bioresour Technol 101(12):4729–4732

    Article  PubMed  CAS  Google Scholar 

  • Haroun-Bouhedja F, Ellouali M, Sinquin C, Boisson-Vidal C (2000) Relationship between sulfate groups and biological activities of fucans. Thromb Res 100(5):453–459

    Article  PubMed  CAS  Google Scholar 

  • Hartzell PL, Millstein J, Lapaglia C (1999) Biofilm formation in hyperthermophilic Archaea. Methods Enzymol 310:335–349

    Article  PubMed  CAS  Google Scholar 

  • Heider SAE, Peters-Wendisch P, Wendisch VF, Beekwilder J, Brautaset T (2014) Metabolic engineering for the microbial production of carotenoids and related products with a focus on the rare C50 carotenoids. Appl Microbiol Biotechnol 98(10):4355–4368

    Article  PubMed  CAS  Google Scholar 

  • Johnson AR (1971) Improved method of hexosamine determination. Anal Biochem 44(2):628–635

    Article  PubMed  CAS  Google Scholar 

  • Krüger M, Blumenberg M, Kasten S, Wieland A, Känel L, Klock JH, Michaelis W, Seifert R (2008) A novel, multi-layered methanotrophic microbial mat system growing on the sediment of the Black Sea. Environ Microbiol 10(8):1934–1947

    Article  PubMed  CAS  Google Scholar 

  • La Gatta A, De Rosa M, Marzaioli I, Busico T, Schiraldi C (2010) A complete hyaluronan hydrodynamic characterization using a size exclusion chromatography-triple detector array system during in vitro enzymatic degradation. Anal Biochem 404(1):21–29

    Article  PubMed  CAS  Google Scholar 

  • Llamas I, Mata JA, Tallon R, Bressollier P, Urdaci MC, Quesada E, Béjar V (2010) Characterization of the exopolysaccharide produced by Salipiger mucosus A3T, a halophilic species belonging to the Alphaproteobacteria, isolated on the Spanish Mediterranean seaboard. Mar Drugs 8(8):2240–2251

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mata JA, Béjar V, Llamas I, Arias S, Bressollier P, Tallon R, Urdaci MC, Quesada E (2006) Exopolysaccharides produced by the recently described halophilic bacteria Halomonas ventosae and Halomonas anticariensis. Res Microbiol 157(9):827–835

    Article  PubMed  CAS  Google Scholar 

  • Nichols CA, Guezennec J, Bowman JP (2005) Bacterial exopolysaccharides from extreme marine environments with special consideration of the southern ocean, sea ice, and deep-sea hydrothermal vents: a review. Mar Biotechnol 7(4):253–271

    Article  PubMed  CAS  Google Scholar 

  • Nicolaus B, Manca MC, Romano I, Lama L (1993) Production of an exopolysaccharide from two thermophilic archaea belonging to the genus Sulfolobus. FEMS Microbiol Lett 109(2–3):203–206

    Article  CAS  Google Scholar 

  • Nicolaus B, Lama L, Esposito E, Manca MC, Improta R, Bellitti MR, Duckworth AW, Grant WD, Gambacorta A (1999) Haloarcula spp. able to biosynthesize exo-endopolymers. J Ind Microbiol Biotechnol 23(6):489–496

    Article  CAS  Google Scholar 

  • Nicolaus B, Panico A, Manca MC, Lama L, Gambacorta A, Maugeri T, Gugliandolo C, Caccamo D (2000) A thermophilic Bacillus isolated from an Eolian shallow hydrothermal vent, able to produce exopolysaccharides. Syst Appl Microbiol 23(3):426–432

    Article  PubMed  CAS  Google Scholar 

  • Nicolaus B, Kambourova M, Oner ET (2010) Exopolysaccharides from extremophiles: from fundamentals to biotechnology. Environ Technol 31(10):1145–1158

    Article  PubMed  CAS  Google Scholar 

  • Paramonov NA, Parolis LA, Parolis H, Boán IF, Antón J, Rodríguez-Valera F (1998) The structure of the exocellular polysaccharide produced by the archaeon Haloferax gibbonsii. Carbohydr Res 309(1):89–94

    Article  PubMed  CAS  Google Scholar 

  • Parolis H, Parolis LA, Boán IF, Rodríguez-Valera F, Widmalm G, Manca MC, Jansson PE, Sutherland IW (1996) The structure of the exopolysaccharide produced by the halophilic Archaeon Haloferax mediterranei strain R4 (ATCC 33500). Carbohydr Res 295:147–156

    Article  PubMed  CAS  Google Scholar 

  • Poli A, Kazak H, Gürleyendağ B, Tommonaro G, Pieretti G, Toksoy Öner E, Nicolaus B (2009) High level synthesis of levan by a novel Halomonas species growing on defined media. Carbohydr Polym 78(4):651–657

    Article  CAS  Google Scholar 

  • Poli A, Anzelmo G, Nicolaus B (2010) Bacterial exopolysaccharides from extreme marine habitats: production, characterization and biological activities. Mar Drugs 8(6):1779–1802

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem 269(2):337–341

    Article  PubMed  CAS  Google Scholar 

  • Priyanka P, Arun AB, Rekha PD (2014) Sulfated exopolysaccharide produced by Labrenzia sp. PRIM-30, characterization and prospective applications. Int J Biol Macromol 69:290–295

    Article  CAS  Google Scholar 

  • Rinker KD, Kelly RM (1996) Growth physiology of the hyperthermophilic archaeon Thermococcus litoralis: development of a sulfur-free defined medium, characterization of an exopolysaccharide, and evidence of biofilm formation. Appl Environ Microbiol 62(12):4478–4485

    PubMed  PubMed Central  CAS  Google Scholar 

  • Saravanan R, Shanmugam A (2010) Isolation and characterization of low molecular weight glycosaminoglycans from marine mollusc Amussium pleuronectus (linne) using chromatography. Appl Biochem Biotechnol 160(3):791–799

    Article  PubMed  CAS  Google Scholar 

  • Senni K, Pereira J, Gueniche F, Delbarre-Ladrat C, Sinquin C, Ratiskol J, Godeau G, Fischer AM, Helley D, Colliec-Jouault S (2011) Marine polysaccharides: a source of bioactive molecules for cell therapy and tissue engineering. Mar Drugs 9(9):1664–1681

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Severina LO, Usenko IA, Plakunov VK (1990) Exopolysaccharide biosynthesis by the extreme halophilic archaebacterium Halobacterium volcanii. Mikrobiologiia 59:437–442

    CAS  Google Scholar 

  • Song YR, Song NE, Kim JH, Nho YC, Baik SH (2011) Exopolysaccharide produced by Bacillus licheniformis strains isolated from Kimchi. J Gen Appl Microbiol 57(3):169–175

    Article  PubMed  CAS  Google Scholar 

  • Spanò A, Gugliandolo C, Lentini V, Maugeri TL, Anzelmo G, Poli A, Nicolaus B (2013) A novel EPS-producing strain of Bacillus licheniformis isolated from a shallow vent off Panarea Island (Italy). Curr Microbiol 67(1):21–29

    Article  PubMed  CAS  Google Scholar 

  • Sun ML, Liu SB, Qiao LP, Chen XL, Pang X, Shi M, Zhang XY, Qin QL, Zhou BC, Zhang YZ, Xie BB (2014) A novel exopolysaccharide from deep-sea bacterium Zunongwangia profunda SM-A87: low-cost fermentation, moisture retention, and antioxidant activities. Appl Microbiol Biotechnol 98(17):7437–7445

    Article  PubMed  CAS  Google Scholar 

  • Sutherland IW (1982) Biosynthesis of microbial exopolysaccharides. Adv Microb Physiol 23:79–150

    Article  PubMed  CAS  Google Scholar 

  • Sutherland IW (1990) Biotechnology of microbial exopolysaccharides, Cambridge study in Biotechnology, vol 9. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Sutherland IW (1999) Polysaccharases in biofilms-source-action-consequences! In: Wingender J, Neu TR, Flemming HC (eds) Microbial extracellular polymeric substances. Springer, Berlin, pp 201–230

    Chapter  Google Scholar 

  • Sutherland IW (2001) Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147(1):3–9

    Article  PubMed  CAS  Google Scholar 

  • Thanan R, Oikawa S, Hiraku Y, Ohnishi S, Ma N, Pinlaor S, Yongvanit P, Kawanishi S, Murata M (2014) Oxidative stress and its significant roles in neurodegenerative diseases and cancer. Int J Mol Sci 16(1):193–217

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thibodeau A (2005) Protecting the skin from environmental stresses with an exopolysaccharide formulation. Cosmet Toiletries 120:81–86

    CAS  Google Scholar 

  • Van Fossen AL, Lewis DL, Nichols JD, Kelly RM (2008) Polysaccharide degradation and synthesis by extremely thermophilic anaerobes. Ann NY Acad Sci 1125:322–337

    Article  CAS  Google Scholar 

  • Ventosa A, Gutierrez MC, Kamekura M, Dyall-Smith ML (1999) Proposal to transfer Halococcus turkmenicus, Halobacterium trapanicum JCM 9743 and strain GSL-11 to Haloterrigena turkmenica gen. nov., comb. nov. Int J Syst Bacteriol 49(1):131–136

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors gratefully acknowledge the Integrated Microscopy Facility of the Institute of Genetics and Biophysics, CNR, Naples, in particular, Dr. Rosarita Tatè.

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The authors declare that they have no competing interests.

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Correspondence to Alessandra Morana.

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Squillaci, G., Finamore, R., Diana, P. et al. Production and properties of an exopolysaccharide synthesized by the extreme halophilic archaeon Haloterrigena turkmenica . Appl Microbiol Biotechnol 100, 613–623 (2016). https://doi.org/10.1007/s00253-015-6991-5

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