Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Characterization and Antioxidant Activity of the Exopolysaccharide Produced by Bacillus amyloliquefaciens GSBa-1

  • Zhao, Wen (Beijing Advanced Innovation Center for Food Nutrition and Human Health, Beijing Technology and Business University (BTBU)) ;
  • Zhang, Jian (Beijing Advanced Innovation Center for Food Nutrition and Human Health, Beijing Technology and Business University (BTBU)) ;
  • Jiang, Yun-Yun (Beijing Advanced Innovation Center for Food Nutrition and Human Health, Beijing Technology and Business University (BTBU)) ;
  • Zhao, Xiao (Beijing Advanced Innovation Center for Food Nutrition and Human Health, Beijing Technology and Business University (BTBU)) ;
  • Hao, Xiao-Na (Beijing Advanced Innovation Center for Food Nutrition and Human Health, Beijing Technology and Business University (BTBU)) ;
  • Li, Liu (Beijing Advanced Innovation Center for Food Nutrition and Human Health, Beijing Technology and Business University (BTBU)) ;
  • Yang, Zhen-Nai (Beijing Advanced Innovation Center for Food Nutrition and Human Health, Beijing Technology and Business University (BTBU))
  • Received : 2018.01.08
  • Accepted : 2018.05.30
  • Published : 2018.08.28
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Abstract

The exopolysaccharide (EPS) produced by Bacillus amyloliquefaciens GSBa-1 was isolated and purified by ethanol precipitation, and DEAE-cellulose and Sepharose CL-6B chromatographies. The molecular mass of the purified EPS was determined to be 54 kDa. Monosaccharide analysis showed that the EPS was composed of predominantly glucose, and it was further confirmed by NMR spectroscopy to be ${\alpha}-glucan$ that consisted of a trisaccharide repeating unit with possible presence of two ${\alpha}-(1{\rightarrow}3)$ and one ${\alpha}-(1{\rightarrow}6)$ glucosidic linkages. Microstructural analysis showed that the EPS appeared as ellipsoid or globose with a smooth surface. The EPS had a degradation temperature at $240^{\circ}C$. Furthermore, the EPS had strong DPPH and hydroxyl radical scavenging activities, and moderate superoxidant anion scavenging and metal ion-chelating activities. This is the first characterization of a glucan produced by B. amyloliquefaciens with strong antioxidant activity. The results of this study suggest the potential of the EPS from B. amyloliquefaciens GSBa-1 to serve as a natural antioxidant for application in functional products.

Keywords

References

  1. Abid Y, Casillo A, Gharsallah H, Joulak I, Lanzetta R, Corsaro MM, et al. 2017. Production and structural characterization of exopolysaccharides from newly isolated probiotic lactic acid bacteria. Int. J. Food Microbiol. 103: 669-675.
  2. Schmid SV, Rehm B. 2015. Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front. Microbiol. 6: 496-502.
  3. Singh A, Singh S. 2004. Organic Chemistry of Natural Products. Campus Books International, New Delhi.
  4. Nwodo UU, Okoh AI. 2012. Bacterial exopolysaccharides: functionality and prospects. Int. J. Food Microbiol. 13: 14002-14015.
  5. Sasikumar K, Kozhummal VD, Devendra L, Nampoothiri KM. 2017. An exopolysaccharide (EPS) from a Lactobacillus plantarum BR2 with potential benefits for making functional foods. Bioresour. Technol. 241: 1152-1156 https://doi.org/10.1016/j.biortech.2017.05.075
  6. Guo Y, Pan D, Li H, Sun Y, Zeng X, Yan B, 2013. Antioxidant and activity of immunomodulatory selenium exopolysaccharide produced by Lactococcus lactis subsp. lactis. Food Chem. 138: 84-89. https://doi.org/10.1016/j.foodchem.2012.10.029
  7. Prado MR, Boller C, Zibetti RGM, Souza D, Pedroso LL, Soccol CR. 2016. Anti-inflammatory and angiogenic activity of polysaccharide extract obtained from Tibetan kefir. Microvasc. Res. 108: 29-33. https://doi.org/10.1016/j.mvr.2016.07.004
  8. Du B, Yang Y, Bian Z, Xu B. 2017. Molecular weight and helix conformation determine intestinal anti-inflammatory effects of exopolysaccharide from Schizophyllum commune. Carbohydr. Polym. 172: 68-77. https://doi.org/10.1016/j.carbpol.2017.05.032
  9. Yan JK, Wang WQ, Li L, Wu JY. 2011. Physiochemical properties and antitumor activities of two ${\alpha}$-glucans isolated from hot water and alkaline extracts of Cordyceps (Cs-HK1) fungal mycelia. Carbohydr. Polym. 4: 753-758
  10. Han Y, Liu E, Liu L, Zhang B, Wang Y, Gui M, et al. 2015. Rheological, emulsifying and thermostability properties of two exopolysaccharides produced by Bacillus amyloliquefaciens LPL061. Carbohydr. Polym. 115: 230-237. https://doi.org/10.1016/j.carbpol.2014.08.044
  11. Malick A, Khodaei N, Benkerroum N, Karboune S. 2017. Production of exopolysaccharides by selected Bacillus strains: optimization of media composition to maximize the yield and structural characterization. Int. J. Biol. Macromol. 102: 539-549. https://doi.org/10.1016/j.ijbiomac.2017.03.151
  12. Chen YT, Yuan Q, Shan LT, Lin MA, Chen DQ, Li CY. 2013. Antitumor activity of bacterial exopolysaccharides from the endophyte Bacillus amyloliquefaciens sp. isolated from Ophiopogon japonicus. Oncol Lett. 5: 1787-1792. https://doi.org/10.3892/ol.2013.1284
  13. Yang H, Deng J, Yuan Y, Fan D, Zhang Y, Zhang R, et al. 2015. Two novel exopolysaccharides from Bacillus amyloliquefaciens C-1: antioxidation and effect on oxidative stress. Curr. Microbiol. 70: 298-306. https://doi.org/10.1007/s00284-014-0717-2
  14. Zhao W, Teng JW, Zhang J, Zhao X, Jiang YY, Yang ZN. 2017. Production of exopolysaccharide by fermentation with Bacillus amyloliquefaciens GSBa-1, its rheological characterization and application. Chin. J. Food Sci. 16: 1-9.
  15. Wang J, Zhao X, Tian Z, Yang Y, Yang Z. 2015. Characterization of an exopolysaccharide produced by Lactobacillus plantarum YW11 isolated from Tibet Kefir. Carbohydr. Polym. 125: 16-25. https://doi.org/10.1016/j.carbpol.2015.03.003
  16. Zhang L, Li Y, Zhao X, Zhang X. 2013. Antioxidant activity of an exopolysaccharide isolated from Lactobacillus plantarum C88. Int. J. Food Microbiol. 54: 270-275.
  17. Wang Y, Li C, Liu P, Ahmed Z, Xiao P, Bai X. 2010. Physical characterization of exopolysaccharide produced by Lactobacillus plantarum KF5 isolated from Tibet kefir. Carbohydr. Polym. 82: 895-903. https://doi.org/10.1016/j.carbpol.2010.06.013
  18. Qiao D, Ke C, Hu B, Luo J, Ye H, Sun Y, et al. 2009. Antioxidant activities of polysaccharides from Hyriopsis cumingii. Carbohydr. Polym.78: 199-204 https://doi.org/10.1016/j.carbpol.2009.03.018
  19. Zhao H, Li J, Zhang J, Wang X, Hao L, Jia L. 2017. Purification, in vitro antioxidant and in vivo anti-aging activities of exopolysaccharides by Agrocybe cylindracea. Int. J. Food Microbiol. 102: 351-357.
  20. Tang W, Dong M, Wang W, Han S, Rui X, Chen X, et al. 2017. Structural characterization and antioxidant property of released exopolysaccharides from Lactobacillus delbrueckii ssp. bulgaricus SRFM-1. Carbohydr. Polym. 173: 654-664. https://doi.org/10.1016/j.carbpol.2017.06.039
  21. Zhao H, Li J, Zhang J, Wang X, Hao L, Jia L. 2017. Purification, in vitro antioxidant and in vivo anti-aging activities of exopolysaccharides by Agrocybe cylindracea. Int. J. Food Microbiol. 102: 351-357.
  22. El-Newary SA, Ibrahim AY, Asker MS, Mahmoud MG, Awady ME. 2017. Production, characterization and biological activities of acidic exopolysaccharide from marine Bacillus amyloliquefaciens 3MS. Asian Pac. J. Trop. Med. 10: 652-662. https://doi.org/10.1016/j.apjtm.2017.07.005
  23. Malick A, Khodaei N, Benkerroum N, Karboune S. 2017. Production of exopolysaccharides by selected Bacillus strains: optimization of media composition to maximize the yield and structural characterization. Int. J. Food Microbiol. 102: 539-549.
  24. Zheng JQ, Wang JZ, Shi CW, Mao DB, He PX, Xu CP. 2014. Characterization and antioxidant activity for exopolysaccharide from submerged culture of Boletus aereus. Process Biochem. 49: 1047-1053. https://doi.org/10.1016/j.procbio.2014.03.009
  25. Singh RP, Shukla MK, Mishra A, Kumari P, Reddy CRK, Jha B. 2011. Isolation and characterization of exopolysaccharides from seaweed associated bacteria Bacillus licheniformis. Carbohydr. Polym. 84: 1019-1026. https://doi.org/10.1016/j.carbpol.2010.12.061
  26. Rani RP, Anandharaj M, Sabhapathy P, Ravindran AD. 2017. Physiochemical and biological characterization of novel exopolysaccharide produced by Bacillus tequilensis FR9 isolated from chicken. Int. J. Food Microbiol. 96: 1-10.
  27. Matsuzaki C, Takagaki C, Tomabechi Y, Forsberg LS, Heiss C, Azadi P, et al. 2017. Structural characterization of the immunostimulatory exopolysaccharide produced by Leuconostoc mesenteroides strain NTM048. Carbohydr. Res. 448: 95-102. https://doi.org/10.1016/j.carres.2017.06.004
  28. Yu L, Xu X, Zhou J, Lv G, Chen J. 2017. Chain conformation and rheological behavior of exopolysaccharide from Bacillus mucilaginosus SM-01. Food Hydrocoll. 65: 165-174. https://doi.org/10.1016/j.foodhyd.2016.11.013
  29. Maina NH, Tenkanen M, Maaheimo H, Juvonen R, Virkki L. 2008. NMR spectroscopic analysis of exopolysaccharides produced by Leuconostoc citreum and Weissella confusa. Carbohydr. Res. 343: 1446-1455. https://doi.org/10.1016/j.carres.2008.04.012
  30. Liu J, Luo J, Ye H, Sun Y, Lu Z, Zeng X. 2010. Medium optimization and structural characterization of exopolysaccharides from endophytic bacterium Paenibacillus polymyxa EJS-3. Carbohydr. Polym. 79: 206-213. https://doi.org/10.1016/j.carbpol.2009.07.055
  31. Bowen WH, Burne RA, Wu H, Koo H. 2017. Oral biofilms: pathogens, matrix, and polymicrobial interactions in microenvironments. Trends Microbiol. 26: 229-242.
  32. Magdalena PB, Adam C, Adam W, Sabina G, Andrzej G, Justyna C. 2015. Physicochemical characterization of exopolysaccharides produced by Lactobacillus rhamnosus on various carbon sources. Carbohydr. Polym. 117: 501-509. https://doi.org/10.1016/j.carbpol.2014.10.006
  33. Liu L, Qin Y, Wang Y, Li H, Shang N, Li P. 2014. Complete genome sequence of Bifidobacterium animalis RH, a probiotic bacterium producing exopolysaccharides. J. Biotechnol. 189: 86-87. https://doi.org/10.1016/j.jbiotec.2014.08.041
  34. Wang K, L i W, R ui X , C hen X, J iang M , Dong M . 2014. Structural characterization and bioactivity of released exopolysaccharides from Lactobacillus plantarum 70810. Int. J. Biol. Macromol. 67: 71-78. https://doi.org/10.1016/j.ijbiomac.2014.02.056
  35. Maina NH, Tenkanen M, Maaheimo H, Juvonen R, Virkki L. 2008. NMR spectroscopic analysis of exopolysaccharides produced by Leuconostoc citreum and Weissella confusa. Carbohydr. Res. 343: 1446-1455. https://doi.org/10.1016/j.carres.2008.04.012
  36. Saravanan C, Shetty PKH. 2016. Isolation and characterization of exopolysaccharide from Leuconostoc lactis KC117496 isolated from idli batter. Int. J. Biol. Macromol. 90: 100-106. https://doi.org/10.1016/j.ijbiomac.2015.02.007
  37. Bounaix MS, Gabriel V, Robert H, Morel S, Remaud-Simeon M, Gabriel B, et al. 2010. Characterization of glucan-producing Leuconostoc strains isolated from sourdough. Int. J. Biol. Macromol. 144: 1-9.
  38. Seymour FR, Knapp RD, Chen ECM, Jeanes A, Bishop SH. 1979. Structural analysis of dextrans containing 2-O-${\alpha}$-Dglucosylated ${\alpha}$-D-glucopyranosyl residues at the branch points, by use of $^{13}C$-nuclear magnetic resonance spectroscopy and gas-liquid chromatography-mass spectrometry. Carbohydr. Res. 71: 231-250. https://doi.org/10.1016/S0008-6215(00)86072-3
  39. Maity P, Nandi AK, Manna DK, Pattanayak M, Sen IK, Bhanja SK, et al. 2017. Structural characterization and antioxidant activity of a glucan from Meripilus giganteus. Carbohydr. Polym. 157: 1237-1245. https://doi.org/10.1016/j.carbpol.2016.11.006
  40. Dertli E, Colquhoun IJ, Cote GL, Le GG, Narbad A. 2018. Structural analysis of the ${\alpha}$-D-glucan produced by the sourdough isolate Lactobacillus brevis E25. Food Chem. 242: 45-52. https://doi.org/10.1016/j.foodchem.2017.09.017
  41. Bounaix MS, Gabriel V, Morel S, Robert H, Rabier P, Remaud-Simeon M, et al. 2009. Biodiversity of exopolysaccharides produced from sucrose by sourdough lactic acid bacteria. J. Agric. Food Chem. 57: 10889-10897. https://doi.org/10.1021/jf902068t
  42. Kodali VP, Dr RS. 2010. Antioxidant and free radical scavenging activities of an exopolysaccharide from a probiotic bacterium. Biotechnol. J. 3: 245-251.
  43. Liu CF, Tseng KC, Chiang SS, Lee BH, Hsu WH, Pan TM. 2011. Immunomodulatory and antioxidant potential of Lactobacillus exopolysaccharides. J. Sci. Food Agric. 91: 2284-2291.
  44. Abdhul K, Ganesh M, Shanmughapriya S, Kanagavel M, Anbarasu K, Natarajaseenivasan K. 2014. Antioxidant activity of exopolysaccharide from probiotic strain Enterococcus faecium (BDU7) from Ngari. Int. J. Biol. Macromol. 70: 450-454. https://doi.org/10.1016/j.ijbiomac.2014.07.026
  45. Adesulu-Dahunsi AT, Sanni AI, Jeyaram K. 2018. Production, characterization and in vitro antioxidant activities of exopolysaccharide from Weissella cibaria GA44. LWT Food Sci. Technol. 87: 432-442. https://doi.org/10.1016/j.lwt.2017.09.013
  46. You L, Gao Q, Feng M, Yang B, Ren J, Gu L, et al. 2013. Structural characterisation of polysaccharides from Tricholoma matsutake and their antioxidant and antitumour activities. Food Chem. 138: 2242-2249. https://doi.org/10.1016/j.foodchem.2012.11.140
  47. Huang Q L, S iu K C , Wang WQ, C heung YC , Wu J Y. 2 010. Fractionation, characterization and antioxidant activity of exopolysaccharides from fermentation broth of a Cordyceps sinensis fungus. Process Biochem. 48: 380-386
  48. Liu J, Luo J, Ye H, Sun Y, Lu Z, Zeng X. 2010. In vitro and in vivo antioxidant activity of exopolysaccharides from endophytic bacterium Paenibacillus polymyxa EJS-3. Carbohydr. Polym. 82: 1278-1283. https://doi.org/10.1016/j.carbpol.2010.07.008
  49. Cao S, Zhan H, Fu SY, Chen L. 2007. Regulation of superoxide anion radical during the oxygen delignification process. Chin. J. Chem. Eng. 15: 132-137. https://doi.org/10.1016/S1004-9541(07)60046-9
  50. Wang X, S hao C , Liu L, G uo X , Xu Y , Lu X . 2017. Optimization, partial characterization and antioxidant activity of an exopolysaccharide from Lactobacillus plantarum KX041. Int. J. Biol. Macromol. 103: 1173-1184. https://doi.org/10.1016/j.ijbiomac.2017.05.118
  51. Tsiapali E, Whaley S, Kalbfleisch J, Ensley HE, Browder IW, Williams DL. 2001. Glucans exhibit weak antioxidant activity, but stimulate macrophage free radical activity. Free Radic. Biol. Med. 30: 393-402 https://doi.org/10.1016/S0891-5849(00)00485-8
  52. Cao J, Zhang H-J, Xu C-P. 2014. Culture characterization of exopolysaccharides with antioxidant activity produced by Pycnoporus sanguineus in stirred-tank and airlift reactors. J. Taiwan Inst. Chem. 45: 2075-2080. https://doi.org/10.1016/j.jtice.2014.05.005
  53. Hussain PR, Rather SA, Suradkar PP. 2018. Structural characterization and evaluation of antioxidant, anticancer and hypoglycemic activity of radiation degraded oat (Avena sativa) ${\beta}$-glucan. Radiat. Phys. Chem. 144: 218-230. https://doi.org/10.1016/j.radphyschem.2017.08.018
  54. Maity P, Sen IK, Maji PK, Paloi S, Devi KSP, Acharya K, et al. 2015. Structural, immunological, and antioxidant studies of ${\beta}$-glucan from edible mushroom Entoloma lividoalbum. Carbohydr. Polym 123: 350-358. https://doi.org/10.1016/j.carbpol.2015.01.051
  55. Liu W, Wang H, Pang X, Yao W, Gao X. 2010. Characterization and antioxidant activity of two lowmolecular-weight polysaccharides purified from the fruiting bodies of Ganoderma lucidum. Int. J. Biol. Macromol. 46: 451-457. https://doi.org/10.1016/j.ijbiomac.2010.02.006
  56. Je JY, Park PJ, Kim EK, Park JS, Yoon HD, Kim KR, et al. 2009. Antioxidant activity of enzymatic extracts from the brown seaweed Undaria pinnatifida by electron spin resonance spectroscopy. LWT Food Sci. Technol. 42: 874-878. https://doi.org/10.1016/j.lwt.2008.10.012
  57. Xu R, Shang N, Li P. 2011. In vitro and in vivo antioxidant activity of exopolysaccharide fractions from Bifidobacterium animalis RH. Anaerobe 17: 226-231. https://doi.org/10.1016/j.anaerobe.2011.07.010
  58. Duh PD. 1999. Antioxidant activity of water extract of four Harng Jyur (Chrysanthemum morifolium Ramat) varieties in soybean oil emulsion. Food Chem. 66: 471-476. https://doi.org/10.1016/S0308-8146(99)00081-3
  59. Yuan YV, Bone DE, Carrington MF. 2005. Antioxidant activity of dulse (Palmaria palmata) extract evaluated in vitro. Food Chem. 91: 485-494. https://doi.org/10.1016/j.foodchem.2004.04.039
  60. Yang H, Deng J, Yuan Y, Fan D, Zhang Y, Zhang R, et al. 2015. Two novel exopolysaccharides from Bacillus amyloliquefaciens C-1: antioxidation and effect on oxidative stress. Curr. Microbiol. 70: 298-306. https://doi.org/10.1007/s00284-014-0717-2
  61. Soeiro VC, Melo KRT, Alves MGCF, Medeiros MJC, Grilo MLPM, Almeidalima J, et al. 2016. Dextran: influence of molecular weight in antioxidant properties and immunomodulatory potential. Int. J. Biol. Macromol. 17:1340-1344
  62. Gao T, Ma S, Song J, Bi H, Tao Y. 2011. Antioxidant and immunological activities of water-soluble polysaccharides from Aconitum kusnezoffii Reichb. Int. J. Biol. Macromol. 49: 580-584. https://doi.org/10.1016/j.ijbiomac.2011.06.017
  63. Li DM, Zhou DY, Zhu BW, Miao L, Qin L, Dong XP, et al. 2013. Extraction, structural characterization and antioxidant activity of polyhydroxylated 1,4-naphthoquinone pigments from spines of sea urchin Glyptocidaris crenularis and Strongylocentrotus intermedius. Eur. Food Res. Technol. 237: 331-339. https://doi.org/10.1007/s00217-013-1996-8
  64. Melo-Silveira RF, Fidelis GP, Viana RL, Soeiro VC, Silva RA, Machado D, et al. 2014. Antioxidant and antiproliferative activities of methanolic extract from a neglected agricultural product: corn cobs. Molecules 19: 5360-5367. https://doi.org/10.3390/molecules19045360

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