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Characterization of an extracellular polysaccharide produced by a Saharan bacterium Paenibacillus tarimensis REG 0201M

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Abstract

The purpose of this paper is to highlight the novel molecular characteristics and rheological properties of the polysaccharide produced by a bacterium isolated from extremophilic environment (Algerian Sahara). Phenotypic and molecular characteristics of the REG 0201M bacterial strain retained for this research were studied. Extracellular polysaccharide produced by REG 0201M was purified, characterized and its production was investigated. Analysis of 16S rDNA gene sequence showed that strain REG 0201M belonged to the species Paenibacillus tarimensis. In sucrose agar medium, 1.31 g dry weight of the polysaccharide per liter was produced. Evaluation of water absorption capacity showed that this polysaccharide was able to absorb 1000 times more water than its own weight. The average molecular weight determined by high-performance size exclusion chromatography multiangle laser light scattering was 1.718 × 106 g mol−1. Analysis of the monosaccharide composition by high-performance anion exchange chromatography showed the presence of fructose (77.67%) as the main neutral sugar, followed by galactose (20.37%), arabinose (1.79%), and rhamnose (0.16%). Its global charge determined by the Zeta potential measurement was about −35.27 ± 0.66 mV. The main functional groups were elucidated by Fourier-Transform Infrared Spectroscopy while the surface morphology was resolved by scanning electron microscopy analysis. Moreover, the rheological data revealed shear thinning properties with the same general behavior of the studied polysaccharide compared to xanthan. These results show the great potential of this polysaccharide, which could help to promote its use in various industries by replacing synthetic polymers.

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References

  • Amellal N, Burtin G, Bartoli F, Heulin T (1998) Colonization of wheat roots by an exopolysaccharide-producing Pantoea agglomerans strain and its effect on rhizosphere soil aggregation. Appl Environ Microbiol 64:3740–3747

    PubMed  CAS  PubMed Central  Google Scholar 

  • Armstrong DC, Johns MR (1997) Culture conditions affect the molecular weight properties of hyaluronic acid produced by Streptococcus zooepidemicus. Appl Environ Microbiol 63:2759–2764

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bajestani MI, Mousavia SM, Jafarib A, Shojaosadati SA (2017) Biosynthesis and physicochemical characterization of a bacterial polysaccharide/polyamide blend, applied for microfluidics study in porous media. Int J Biol Macromol 96:100–110

    Article  PubMed  CAS  Google Scholar 

  • Banat IM, Franzetti A, Gandolfi I, Bestetti G, Martinotti MG, Fracchia L, Smyth TJ, Marchant R (2010) Microbial biosurfactants production, applications and future potential. Appl Microbiol Biotechnol 87:427–444

    Article  PubMed  CAS  Google Scholar 

  • Berwanger AL, Da S, Scamparini ARP, Domingues NM, Vanzo LT, Treichel H, Padilha FF (2007) Produção de biopolímero sintetizado por Sphingomonas capsulata a partir de meios industriais. Ciênc Agrotecnol 31:177–183

    Article  CAS  Google Scholar 

  • Byrom D (1987) Polymer synthesis by micro-organisms: technology and economics. Trends Biotechnol 5:246–250

    Article  CAS  Google Scholar 

  • Calero N, Muñoz J, Ramírez P, Guerrero A (2010) Flow behaviour, linear viscoelasticity and surface properties of chitosan aqueous solutions. Food Hydrocoll 24:659–666

    Article  CAS  Google Scholar 

  • Cross MM (1965) Rheology of non-Newtonian fluids. A new flow equation for pseudo-plastic systems. J Colloid Sci 20:417–437

    Article  CAS  Google Scholar 

  • De Vos P, Ludwig W, Schleifer KH, Whitman WB (2015) Chapter introduction: “Paenibacillaceae” fam. nov. In: Whitman WB (ed) Bergey’s manual of systematics of archaea and bacteria. John Wiley and Sons. https://doi.org/10.1002/9781118960608.fbm00114

  • Donot F, Fontana A, Baccou JC, Schorr-Galindo S (2012) Microbial exopolysaccharides: Main examples of synthesis, excretion, genetics and extraction. Carbohydr Polym 87:951–962

    Article  CAS  Google Scholar 

  • Dunstan DE, Hill EK, Wei Y (2004) Direct measurement of polymer segment orientation and distortion in shear: semi dilute solution behavior. Polymer 45:1261–1266

    Article  CAS  Google Scholar 

  • Ebagninin KW, Benchabane A, Bekkour K (2009) Rheological characterization of poly (ethylene oxide) solutions of different molecular weights. J Colloid Interface Sci 336:360–367

    Article  PubMed  CAS  Google Scholar 

  • Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes Appl. Environ Microbiol 74:2461–2470

    Article  CAS  Google Scholar 

  • Freitas F, Alves VD, Carvalheira M, Costa N, Oliveira R, Reis MA (2009) Emulsifying behaviour and rheological properties of the extracellular polysaccharide produced by Pseudomonas oleovorans grown on glycerol by product. Carbohydr Polym 78:549–556

    Article  CAS  Google Scholar 

  • Gamar L, Blondeau K, Simonet JM (1997) Physiological approach to extracellular polysaccharide production by Lactobacillus rhamnosus strain C83. J Appl Microbial 83:281–287

    Article  CAS  Google Scholar 

  • Grady EN, MacDonald J, Liu L, Richman A, Yuan ZC (2016) Current knowledge and perspectives of Paenibacillus: a review. Microb Cell Factories 15:203

    Article  Google Scholar 

  • Gugliandolo C, Spanò A, Maugeri TL, Poli A, Arena A, Nicolaus B (2015) Role of bacterial exopolysaccharides as agents in counteracting immune disorders induced by herpes virus. Microorganisms 3(3):464–483

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Guilherme MR, Aouada FA, Fajardo AR, Martins AF, Paulino AT, Davi MFT, Rubira AF, Muniz EC (2015) Superabsorbent hydrogels based on polysaccharides for application in agriculture as soil conditioner and nutrient carrier: a review. Eur Polym J 72:365–385

    Article  CAS  Google Scholar 

  • Han Y, Liu E, Liu L, Zhang B, Wang Y, Gui M, Wu R, Li P (2015) Rheological, emulsifying and thermostability properties of two exopolysaccharides produced by Bacillus amyloliquefaciens LPL061. Carbohydr Polym 115:230–237

    Article  PubMed  CAS  Google Scholar 

  • Hwang HJ, Kima SW, Choi JW, Yun JW (2003) Production and characterization of exopolysaccharides from submerged culture of Phellinus linteus KCTC 6190. Enzym Microb Technol 33:309–319

    Article  CAS  Google Scholar 

  • Iyer A, Mody K, Jha B (2005) Characterization of an exopolysaccharide produced by a marine Enterobacter cloacae. Indian J Exp Biol 43:467–471

    PubMed  CAS  Google Scholar 

  • Janczarek M, Jaroszuk-S’ciseł J, Skorupska A (2009) Multiple copies of rosR and pssA genes enhance exopolysaccharide production, symbiotic competitiveness and clover nodulation in Rhizobium leguminosarum bv. trifolii. Antonie Van Leeuwenhoek 96:471–486

    Article  PubMed  CAS  Google Scholar 

  • Johns MR, Noor E (1991) Recovery and purification of polysaccharides from microbial broth. Aust J Biotechnol 5:73–77

    PubMed  CAS  Google Scholar 

  • Jung HK, Hong JH, Park SC, Park BK, Nam DH, Kim SD (2007) Production and physicochemical characterization of β-glucan produced by Paenibacillus polymyxa JB115. Biotechnol Bioprocess Eng 12:713–719

    Article  CAS  Google Scholar 

  • Kaci Y, Heyraud A, Barakat M, Heulin T (2005) Isolation and identification of an EPS-producing Rhizobium strain from arid soil (Algeria): characterization of its EPS and the effect of inoculation on wheat rhizosphere soil structure. Res Microbiol 156:522–531

    Article  PubMed  CAS  Google Scholar 

  • Karbowiak T, Ferret E, Debeaufort F, Voilley A, Cayot P (2011) Investigation of water transfer across thin layer biopolymer films by infrared spectroscopy. J Membr Sci 370:82–90

    Article  CAS  Google Scholar 

  • Kavita K, Singh VK, Mishraa A, Jha B (2014) Characterisation and anti-biofilm activity of extracellular polymeric substances from Oceanobacillus iheyensis. Carbohydr Polym 101:29–35

    Article  PubMed  CAS  Google Scholar 

  • Kenyon WJ, Esch SW, Buller CS (2005) The curdlan-type exopolysaccharide produced by Cellulomonas flavigena KU forms part of an extracellular glycocalyx involved in cellulose degradation. Anton Leeuw 87:143–148

    Article  CAS  Google Scholar 

  • Kilic NK, Dönmez G (2008) Environmental conditions affecting exopolysaccharide production by Pseudomonas aeruginosa, Micrococcus sp., and Ochrobactrum sp. J Hazard Mat 154:1019–1024

    Article  CAS  Google Scholar 

  • Lai LS, Tung J, Lin PS (2000) Solution properties of hsian-tsao (Meaonaprocumbens) leaf gum. Food Hydrocoll 14:287–294

    Article  CAS  Google Scholar 

  • Lapasin R, De Lorenzi L, Pricl S, Torriano G (1995) Flow properties of hydrox-ypropyl guar gum and its long-chain hydrophobic derivatives. Carbohydr Polym 28:195–202

    Article  CAS  Google Scholar 

  • Lee HC, Brant DA (2002) Rheology of concentrated isotropic and anisotropic xanthan solutions. 1. A rodlike low molecular weight sample. Macromol 35:2212–2222

    Article  CAS  Google Scholar 

  • Liang TW, Wang SL (2015) Exopolysaccharides from Paenibacillus spp: production, isolation, structure, and bioactivities. Mar Drugs 13:1847–1863

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Liu J, Luo J, Ye H, Sun Y, Lu Z, Zeng X (2009) Production, characterization and antioxidant activities in vitro of exopolysaccharides from endophytic bacterium Paenibacillus polymyxa EJS-3. Carbohydr Polym 78:275–281

    Article  CAS  Google Scholar 

  • Moshabaki Isfahani F, Tahmourespour A, Hoodaji M, Ataabadi M, Mohammadi A (2018) Characterizing the new bacterial isolates of high yielding exopolysaccharides under hypersaline conditions. J Clean Prod 185:922–928

    Article  CAS  Google Scholar 

  • Muller FL, Pain JP, Villion P (1994) On the behaviour of non-Newtonian liquids in collinear ohmic heaters, In Proceedings of the 10th international heat transfer conference, freezing, melting, internal forces convection and heat exhchangers, vol. 4. Brighton, UK, p 285–290

  • Nazia J, Nuzhat A (2008) Production of biopolymers by Pseudomonas aeruginosa isolated from marine source. Braz Arch Biol Technol 51:457–464

    Article  Google Scholar 

  • Nicolaus B, Lama L, Panico A, Schiano Moriello V, Romano I, Gambacorta A (2002) Production and characterization of exopolysaccharides excreted by thermophilic bacteria from shallow, marine hydrothermal vents of flegrean areas (Italy). Syst Appl Microbiol 25:319–325

    Article  PubMed  CAS  Google Scholar 

  • Nouha K, Hoang NV, Tyagi RD (2016) Fourier transform infrared spectroscopy and liquid chromatography mass spectrometry study of extracellular polymer substances produced on secondary sludge fortified with crude glycerol. J Mat Sci Eng 5:3

    Google Scholar 

  • Öner ET (2013) Chapter 2: microbial production of extracellular polysaccharides from biomass. In: Fang Z (ed) Pretreatment techniques for biofuels and biorefineries. p 35–56. https://doi.org/10.1007/978-3-642-32735-3_2

  • Ostwald W, Auerbach R (1926) The viscosity of colloidal solutions in the area of structure, laminar and turbulence. Kolloidn Zh 38:261–280

    Article  CAS  Google Scholar 

  • Paul F, Morin A, Monsan P (1986) Microbial polysaccharides with actual potential industrial applications. Biotech Adv 4:245–259

    Article  CAS  Google Scholar 

  • Rafigh SM, Yazdi AV, Vossoughi M, Safekordi AA, Ardjmand M (2014) Optimization of culture medium and modeling of curdlan production from Paenibacillus polymyxa by RSM and ANN. Int J Biol Macromol 70:463–473

    Article  PubMed  CAS  Google Scholar 

  • Raguénès G, Pignet P, Gauthier G, Peres A, Christen R, Rougeaux H, Barbier G, Guezennec J (1996) Description of a new polymer-secreting bacterium from a deep-sea hydrothermal vent, Alteromonas macleodii subsp. fijiensis, and preliminary characterization of the polymer. Appl Environ Microbiol 62:67–73

    PubMed  PubMed Central  Google Scholar 

  • Rani RP, Anandharaj M, Ravindran AD (2018) Characterization of a novel exopolysaccharide produced by Lactobacillus gasseri FR4 and demonstration of its in vitro biological properties. Int J Biol Macromol 109:772–783

    Article  PubMed  CAS  Google Scholar 

  • Rättö M, Suihko ML, Siika-aho M (2005) Polysaccharide-producing bacteria isolated from paper machine slime deposits. J Ind Microbiol Biotechnol 32:109–114

    Article  PubMed  CAS  Google Scholar 

  • Raza W, Makeen K, Wang Y, Xu Y, Qirong S (2011) Optimization, purification, characterization and antioxidant activity of an extracellular polysaccharide produced by Paenibacillus polymyxa SQR-21. Bioresour Technol 102:6095–6103

    Article  PubMed  CAS  Google Scholar 

  • Rinaudo M, Milas M (1982) Xanthan properties in aqueous solution. Carbohydr Polym 2:264–269

    Article  CAS  Google Scholar 

  • Rioux LE, Turgeon SL, Beaulieu M (2007) Characterization of polysaccharides extracted from brown seaweeds. Carbohydr Polym 69:530–537

    Article  CAS  Google Scholar 

  • Ryuichiro K, Nohata Y (1994) A new water absorbing polysaccharide from Alcaligenes latus. Biosci Biotechnol Biochem 58:235–238

    Article  Google Scholar 

  • San-Blas E, Cubillánb N, Guerrac M, Portillo E, Esteves I (2012) Characterization of Xenorhabdus and Photorhabdus bacteria by Fourier transform mid-infrared spectroscopy with attenuated total reflection (FT-IR/ATR). Spectrochim Acta A 93:58–62

    Article  CAS  Google Scholar 

  • Smoluchowski VM (1916) Theoretical observations on the viscosity of colloides. Kolloidn Zh 18:190–195

    Article  Google Scholar 

  • Sochi T (2010) Non-Newtonian flow in porous media. Polymer 51(22):5007–5023

    Article  CAS  Google Scholar 

  • Sutherland IW (1994) Structure-function relationships in microbial exopolysaccharides, biotechnology advances. Biotechnol Adv 12:393–448

    Article  PubMed  CAS  Google Scholar 

  • Taguett F, Boisset C, Heyraud A, Buon L, Kaci Y (2015) Characterization and structure of the polysaccharide produced by Pseudomonas fluorescens strain TF7 isolated from an arid region of Algeria. C R Biol 338:335–342

    Article  PubMed  Google Scholar 

  • Trabelsi I, Ktari N, Triki M, Bkhairia I, Ben Slima S, Sassi Aydi S, Aydi S, Abdeslam A, Ben Salah R (2018) Physicochemical, techno-functional, and antioxidant properties of a novel bacterial exopolysaccharide in cooked beef sausage. Int J Biol Macromol 111:11–18

    Article  PubMed  CAS  Google Scholar 

  • Wang M, Yang M, Zhou G, Luo X, Zhang L, Tang Y, Fang C (2008) Paenibacillus tarimensis sp. nov., isolated from sand in Xinjiang, China. Int J Syst Evol Microbiol 58:2081–2085

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Ding S, Wang G, Xu X, Zhou G (2013) In situ characterization and analysis of Salmonella biofilm formation under meat processing environments using a combined microscopic and spectroscopic approach. Int J Food Microbiol 167:293–302

    Article  PubMed  CAS  Google Scholar 

  • Wei X, Fang L, Cai P, Huang Q, Chen H, Liang W, Rong X (2011) Influence of extracellular polymeric substances (EPS) on Cd adsorption by bacteria. Environ Pollut 159(5):1369–1374

    Article  PubMed  CAS  Google Scholar 

  • Xiu A, Zhou M, Zhu B, Wang S, Zhang J (2011) Rheological properties of Salecan as a new source of thickening agent. Food Hydrocoll 25:1719–1725

    Article  CAS  Google Scholar 

  • Xu C, Willför S, Holmlund P, Holmbom B (2009) Rheological properties of water-soluble spruce O-acetyl galactoglucomannans. Carbohydr Polym 75:498–504

    Article  CAS  Google Scholar 

  • Xu X, Gao C, Liu Z, Wu J, Han J, Yan M, Wu Z (2016) Characterization of the levan produced by Paenibacillus bovis sp. nov BD3526 and its immunological activity. Carbohydr Polym 144:178–186

    Article  PubMed  CAS  Google Scholar 

  • Ye L, Zhang J, Yang Y, Zhou S, Liu Y, Tang Q (2009) Structural characterization of a heteropolysaccharide by NMR spectra. Food Chem 112:962–966

    Article  CAS  Google Scholar 

  • Yu L, Xu S, Deng C, Li H, Yang Q, Xu Z, Chen J (2016) Preparation and partial structural characterization of the exopolysaccharide from Bacillus mucilaginosus SM-01. Carbohydr Polym 146:217–223

    Article  PubMed  CAS  Google Scholar 

  • Zhou F, Wu Z, Chen C, Han J, Ai L, Guo B (2014) Exopolysaccharides produced by Rhizobium radiobacter S10 in whey and their rheological properties. Food Hydrocoll 36:362–368

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are very grateful to Professor Sylvie Turgeon, Doctor Laurie-Eve Rioux and Diane Gagnon (Department of Food Science and Nutrition, Institute of Nutrition and Functional Food, Laval University, Quebec, Canada) for their valuable advice and technical assistance in Molecular weight determination and Rheological study of polysaccharides.

We would like to thank Claire Boisset (CNRS, CERMAV, Grenoble-France) for technical assistance in HPAEC-Dionex. We would like to thank Kamel Ait Messaoud and Okba Selama for providing language assistance.

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  1. Laboratory of Organism Physiology and Biology, Team of Soil Biology, Faculty of Biological Science, USTHB, BP 32, Algiers, EL Alia, Algeria

    Nadia Boukhelata, Farida Taguett & Yahia Kaci

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  1. Nadia Boukhelata
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  2. Farida Taguett
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Correspondence to Yahia Kaci.

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Boukhelata, N., Taguett, F. & Kaci, Y. Characterization of an extracellular polysaccharide produced by a Saharan bacterium Paenibacillus tarimensis REG 0201M. Ann Microbiol 69, 93–106 (2019). https://doi.org/10.1007/s13213-018-1406-3

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