Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Characterization and Antioxidant Activity of Released Exopolysaccharide from Potential Probiotic Leuconostoc mesenteroides LM187

  • Zhang, Qing (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Wang, Jie (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Sun, Qing (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Zhang, Shu-Ming (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Sun, Xiang-Yang (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Li, Chan-Yuan (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Zheng, Miao-Xin (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Xiang, Wen-Liang (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Tang, Jie (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University)
  • Received : 2021.03.31
  • Accepted : 2021.06.08
  • Published : 2021.08.28
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Abstract

A released exopolysaccharide (rEPS)-producing strain (LM187) with good acid resistance, bile salt resistance, and cholesterol-lowering properties was isolated from Sichuan paocai and identified as Leuconostoc mesenteroides subsp. mesenteroides. The purified rEPS, designated as rEPS414, had a uniform molecular weight of 7.757 × 105 Da. Analysis of the monosaccharide composition revealed that the molecule was mainly composed of glucose. The Fourier transform-infrared spectrum showed that rEPS414 contained both α-type and β-type glycosidic bonds. 1H and 13C nuclear magnetic resonance spectra analysis showed that the purified rEPS contained arabinose, galactose, and rhamnose, but less uronic acid. Scanning electron microscopy demonstrated that the exopolysaccharide displayed a large number of scattered, fluffy, porous cellular network flake structures. In addition, rEPS414 exhibited strong in vitro antioxidant activity. These results showed that strain LM187 and its rEPS are promising probiotics with broad prospects in industry.

Keywords

Acknowledgement

This work was supported by the Science and Technology Support Project of Sichuan Province (Grant no. 2019ZYZF0170); the Foundation of Education Department of Sichuan Province (Grant no. 18ZA0447); and the Young Scholars Program of Xihua University.

References

  1. LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M. 2013. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr. Opin. Biotechnol. 24: 160-168. https://doi.org/10.1016/j.copbio.2012.08.005
  2. Zhu Y, Wang X, Pan W, Shen X, He Y, Yin H, et al. 2019. Exopolysaccharides produced by yogurt-texture improving lactobacillus plantarum RS20D and the immunoregulatory activity. Int. J. Biol. Macromol. 121: 342-349. https://doi.org/10.1016/j.ijbiomac.2018.09.201
  3. Laino J, Villena J, Kanmani P, Kitazawa H. 2016. Immunoregulatory effects triggered by lactic acid bacteria exopolysaccharides: new insights into molecular interactions with host cells. Microorganisms 4: 27. https://doi.org/10.3390/microorganisms4030027
  4. Moslehi-Jenabian S, Lindegaard L, Jespersen L. 2010. Beneficial effects of pobiotic and food borne yeasts on human health. Nutrients 2: 449-473. https://doi.org/10.3390/nu2040449
  5. Jin H, Jeong Y, Yoo SH, Johnston TV, Ku S, Ji GE. 2019. Isolation and characterization of high exopolysaccharide-producing Weissella confusa VP30 from young children's feces. Microb. Cell Fact. 18: 110. https://doi.org/10.1186/s12934-019-1158-1
  6. Vinogradov E, Sadovskaya I, Grard T, Chapot-Chartier MP. 2016. Structural studies of the rhamnose-rich cell wall polysaccharide of Lactobacillus casei BL23. Carbohydr. Res. 435: 156-161. https://doi.org/10.1016/j.carres.2016.10.002
  7. Rajoka MSR, Mehwish HM, Hayat HF, Hussain N, Sarwar S, Aslam H, et al. 2019. Characterization, the antioxidant and antimicrobial activity of exopolysaccharide isolated from poultry origin lactobacilli. Probiotics Antimicrob. Proteins 11: 1132-1142. https://doi.org/10.1007/s12602-018-9494-8
  8. Adesulu-Dahunsi AT, Sanni AI, Jeyaram K. 2018. Production, characterization and in vitro antioxidant activities of exopolysaccharide from Weissella cibaria GA44. L.W.T. Food Sci. Technol. 87: 432-442. https://doi.org/10.1016/j.lwt.2017.09.013
  9. You X, Yang L, Zhao X, Ma K, Chen X, Zhang C, et al. 2020. Isolation, purification, characterization and immunostimulatory activity of an exopolysaccharide produced by Lactobacillus pentosus LZ-R-17 isolated from Tibetan kefir. Int. J. Biol. Macromol. 158: 408-419. https://doi.org/10.1016/j.ijbiomac.2020.05.027
  10. Ryan PM, Stolte EH, London LEE, Wells JM, Long SL, Joyce SA, et al. 2019. Lactobacillus mucosae DPC 6426 as a bile-modifying and immunomodulatory microbe. BMC Microbiol. 19: 33. https://doi.org/10.1186/s12866-019-1403-0
  11. Di W, Zhang L, Wang S, Yi H, Han X, Fan R, et al. 2017. Physicochemical characterization and antitumour activity of exopolysaccharides produced by Lactobacillus casei SB27 from yak milk. Carbohydr. Polym. 171: 307-315. https://doi.org/10.1016/j.carbpol.2017.03.018
  12. Li W, Xia X, Tang W, Ji J, Rui X, Chen X, et al. 2015. Structural characterization and anticancer activity of cell-bound exopolysaccharide from Lactobacillus helveticus MB2-1. J. Agric. Food Chem. 63: 3454-3463. https://doi.org/10.1021/acs.jafc.5b01086
  13. Ibarburu I, Puertas AI, Berregi I, Rodriguez-Carvajal MA, Prieto A, Duenas MT. 2015. Production and partial characterization of exopolysaccharides produced by two Lactobacillus suebicus strains isolated from cider. Int. J. Food Microbiol. 214: 54-62. https://doi.org/10.1016/j.ijfoodmicro.2015.07.012
  14. Olivares-Illana V, Lopez-Munguia A, Olvera C. 2003. Molecular characterization of inulosucrase from Leuconostoc citreum: a fructosyltransferase within a glucosyltransferase. J. Bacteriol. 185: 3606-3612. https://doi.org/10.1128/JB.185.12.3606-3612.2003
  15. Rehman R, Wang Y, Wang J, Geng W. 2018. Physicochemical analysis of Mozzarella cheese produced and developed by the novel EPS-producing strain Lactobacillus kefiranofaciens ZW3. Int. J. Dairy Technol. 71: 90-98. https://doi.org/10.1111/1471-0307.12445
  16. Cao J, Yang J, Hou Q, Xu H, Zheng Y, Zhang H, et al. 2017. Assessment of bacterial profiles in aged, home-made Sichuan paocai brine with varying titratable acidity by PacBio SMRT sequencing technology. Food Control 78: 14-23. https://doi.org/10.1016/j.foodcont.2017.02.006
  17. Liu T, Zhou K, Yin S, Liu S, Zhu Y, Yang Y, et al. 2019. Purification and characterization of an exopolysaccharide produced by Lactobacillus plantarum HY isolated from home-made Sichuan Pickle. Int. J. Biol. Macromol. 134: 516-526. https://doi.org/10.1016/j.ijbiomac.2019.05.010
  18. Hu X, Pang X, Wang PG, Chen M. 2019. Isolation and characterization of an antioxidant exopolysaccharide produced by Bacillus sp. S-1 from Sichuan pickles. Carbohydr. Polym. 204: 9-16. https://doi.org/10.1016/j.carbpol.2018.09.069
  19. Miao M, Bai A, Jiang B, Song Y, Cui SW, Zhang T. 2014. Characterisation of a novel water-soluble polysaccharide from Leuconostoc citreum SK24.002. Food Hydrocoll. 36: 265-272. https://doi.org/10.1016/j.foodhyd.2013.10.014
  20. Vinderola CG, Reinheimer JA. 2003. Lactic acid starter and probiotic bacteria: a comparative "in vitro" study of probiotic characteristics and biological barrier resistance. Food Res. Int. 36: 895-904. https://doi.org/10.1016/S0963-9969(03)00098-X
  21. Dilna SV, Surya H, Aswathy RG, Varsha KK, Sakthikumar DN, Pandey A, Nampoothiri KM. 2015. Characterization of an exopolysaccharide with potential health-benefit properties from a probiotic Lactobacillus plantarum RJF4. L.W.T. Food Sci. Technol. 64: 1179-1186. https://doi.org/10.1016/j.lwt.2015.07.040
  22. Mirlohi M, Madany G, Hassanzade A. Yahay MJ. 2011. On the colorimetric method for cholesterol determination in the laboratory media. Int. J. Biol. Chem. 6: 37-41. https://doi.org/10.3923/ijbc.2012.37.41
  23. Savadogo A, Ouattara CAT, Savadogo PW, Barro N, Ouattara AS, Traore AS. 2003. Identification of exopolysaccharides-producing lactic acid bacteria from Burkina Faso fermented milk samples. Afr. J. Biotechnol. 3: 189-194. https://doi.org/10.5897/AJB2004.000-2034
  24. Ruhmann B, Schmid J, Sieber V. 2015. Methods to identify the unexplored diversity of microbial exopolysaccharides. Front. Microbiol. 6: 565. https://doi.org/10.3389/fmicb.2015.00565
  25. Wang K, Niu M, Song D, Song X, Zhao J, Wu Y, et al. 2020. Preparation, partial characterization and biological activity of exopolysaccharides produced from Lactobacillus fermentum S1. J. Biosci. Bioeng. 129: 206-214. https://doi.org/10.1016/j.jbiosc.2019.07.009
  26. Xue BL, Wen JL, Xu F, Sun RC. 2012. Structural characterization of hemicelluloses fractionated by graded ethanol precipitation from Pinus yunnanensis. Carbohydr. Res. 352: 159-165. https://doi.org/10.1016/j.carres.2012.02.004
  27. Li C, Fu X, Luo F, Huang Q. 2013. Effects of maltose on stability and rheological properties of orange oil-in-water emulsion formed by OSA modified starch. Food Hydrocoll. 32: 79-86. https://doi.org/10.1016/j.foodhyd.2012.12.004
  28. Wang L, Liu F, Wang A, Yu Z, Xu Y, Yang Y. 2017. Purification, characterization and bioactivity determination of a novel polysaccharide from pumpkin (Cucurbita moschata) seeds. Food Hydrocoll. 66: 357-364. https://doi.org/10.1016/j.foodhyd.2016.12.003
  29. Rai AK, Jini R, Swapna HC, Sachindra NM, Bhaskar N, Baskaran V. 2011. Application of native lactic acid bacteria (LAB) for fermentative recovery of lipids and proteins from fish processing wastes: bioactivities of fermentation products. J. Aquat. Food Prod. Technol. 20: 32-44. https://doi.org/10.1080/10498850.2010.528174
  30. Xia Z. 2015. Preparation of the oligosaccharides derived from Flammulina velutipes and their antioxidant activities. Carbohydr. Polym. 118: 41-43. https://doi.org/10.1016/j.carbpol.2014.10.074
  31. Feng K, Chen W, Sun L, Liu J, Zhao Y, Li L, et al. 2015. Optimization extraction, preliminary characterization and antioxidant activity in vitro of polysaccharides from Stachys sieboldii Miq. Tubers. Carbohydr. Polym. 125: 45-52. https://doi.org/10.1016/j.carbpol.2015.02.026
  32. Sawa N, Okamura K, Zendo T, Himeno K, Nakayama J, Sonomoto K. 2010. Identification and characterization of novel multiple bacteriocins produced by Leuconostoc pseudomesenteroides QU15. J. Appl. Microbiol. 109: 282-291. https://doi.org/10.1111/j.1365-2672.2009.04653.x
  33. Shevtsov AB, Kushugulova AR, Kojakhmetov SS, Oralbaeva SS, Stoyanova LG, Abzhalelov AB, et al. 2011. Detection of Lactobacillus species using a gene fragment of the RNA polymerase beta subunit rpoB. Moscow Univ. Biol. Sci. Bull. 66: 22-27. https://doi.org/10.3103/S0096392511010093
  34. Angmo K, Kumari A, Savitri, Bhalla TC. 2016. Probiotic characterization of lactic acid bacteria isolated from fermented foods and beverage of Ladakh. LWT Food Sci. Technol. 66: 428-435. https://doi.org/10.1016/j.lwt.2015.10.057
  35. Song M, Yun B, Moon JH, Park DJ, Lim K, Oh S. 2015. Characterization of selected Lactobacillus strains for use as probiotics. Korean J. Food Sci. Anim. Resour. 35: 551-556. https://doi.org/10.5851/kosfa.2015.35.4.551
  36. Guo XH, Kim JM, Namb HM, Park SY, Kim JM. 2010. Screening lactic acid bacteria from swine origins for multistrain probiotics based on in vitro functional properties. Anaerobe 16: 321-326. https://doi.org/10.1016/j.anaerobe.2010.03.006
  37. Succi M, Tremonte P, Reale A, Sorrentino E, Grazia L, Pacifico S, et al. 2005. Bile salt and acid tolerance of Lactobacillus rhamnosus strains isolated from Parmigiano Reggiano cheese. FEMS Microbiol. Lett. 244: 129-137. https://doi.org/10.1016/j.femsle.2005.01.037
  38. Nami Y, Panahi B, Jalaly HM, Bakhshayesh RV, Hejazi MA. 2020. Application of unsupervised clustering algorithm and heat-map analysis for selection of lactic acid bacteria isolated from dairy samples based on desired probiotic properties. L.W.T. Food Sci. Technol. 118: 108839. https://doi.org/10.1016/j.lwt.2019.108839
  39. Lee S, Kim M. 2019. Leuconostoc mesenteroides MKSR isolated from kimchi possesses α-glucosidase inhibitory activity, antioxidant activity, and cholesterol-lowering effects. LWT. 116: 108570. https://doi.org/10.1016/j.lwt.2019.108570
  40. Bhat B, Bajaj BK. 2018. Hypocholesterolemic and bioactive potential of exopolysaccharide from a probiotic Enterococcus faecium K1 isolated from kalarei. Bioresour. Technol. 254: 264-267. https://doi.org/10.1016/j.biortech.2018.01.078
  41. Wang J, Zhao X, Yang Y, Zhao A, Yang Z. 2015. Characterization and bioactivities of an exopolysaccharide produced by Lactobacillus plantarum YW32. Int. J. Biol. Macromol. 74: 119-126. https://doi.org/10.1016/j.ijbiomac.2014.12.006
  42. 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
  43. Wang K, Li W, Rui X, Chen X, Jiang M, Dong M. 2014. Characterization of a novel exopolysaccharide with antitumor activity from Lactobacillus plantarum 70810. Int. J. Biol. Macromol. 63: 133-139. https://doi.org/10.1016/j.ijbiomac.2013.10.036
  44. Sun L, Wang L, Li J, Liu H. 2014. Characterization and antioxidant activities of degraded polysaccharides from two marine Chrysophyta. Food Chem. 160: 1-7. https://doi.org/10.1016/j.foodchem.2014.03.067
  45. Zheng JQ, Mao XJ, Geng LJ, Yang GM, Xu CP. 2014. Production optimization, preliminary characterization and bioactivity of exopolysaccharides from Incutis tamaricis (Pat.) Fiasson & Niemela. J. Taiwan Inst. Chem. Eng. 45: 725-733. https://doi.org/10.1016/j.jtice.2013.08.006
  46. 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. Biol. Macromol. 96: 1-10. https://doi.org/10.1016/j.ijbiomac.2016.11.122
  47. Das D, Goyal A. 2014. Characterization and biocompatibility of glucan: a safe food additive from probiotic Lactobacillus plantarum DM5. J. Sci. Food Agric. 94: 683-690. https://doi.org/10.1002/jsfa.6305
  48. Yu XH, Liu Y, Wu XL, Liu LZ, Fu W, Song DD. 2017. Isolation, purification, characterization and immunostimulatory activity of polysaccharides derived from American ginseng. Carbohydr. Polym. 156: 9-18. https://doi.org/10.1016/j.carbpol.2016.08.092
  49. Walia M, Sharma U, Bhushan S, Kumar N, Singh B. 2013. Arabinan-type polysaccharides from industrial apple pomace waste. Chem. Nat. Compd. 49: 794-798. https://doi.org/10.1007/s10600-013-0750-6
  50. Wu Y, Hu N, Pan Y, Zhou L, Zhou X. 2007. Isolation and characterization of a mannoglucan from edible Cordyceps sinensis mycelium. Carbohydr. Res. 342: 870-875. https://doi.org/10.1016/j.carres.2007.01.005
  51. Wang L, Liu HM, Qin GY. 2017. Structure characterization and antioxidant activity of polysaccharides from Chinese quince seed meal. Food Chem. 234: 314-322. https://doi.org/10.1016/j.foodchem.2017.05.002
  52. Xu YM, Cui YL, Wang X, Yue FF, Shan YY, Liu BF, et al. 2019. Purification, characterization and bioactivity of exopolysaccharides produced by Lactobacillus plantarum KX041. Int. J. Biol. Macromol. 128: 480-492. https://doi.org/10.1016/j.ijbiomac.2019.01.117
  53. Bomfim VB, Neto JHPL, Leite KS, Vieira EDA, Iacomini M, Silva CM, Santos KMOD, et al. 2020. Partial characterization and antioxidant activity of exopolysaccharides produced by Lactobacillus plantarum CNPC003. LWT. 127: 109349. https://doi.org/10.1016/j.lwt.2020.109349
  54. Jiang C, Wang M, Liu J, Gan D, Zeng X. 2011. Extraction, preliminary characterization, antioxidant and anticancer activities in vitro of polysaccharides from Cyclina sinensis. Carbohydr. Polym. 84: 851-857. https://doi.org/10.1016/j.carbpol.2010.11.027
  55. Zhu HJ, Tian L, Zhang L, Bi JX, Song QQ, Yang H, et al. 2018. Preparation, characterization and antioxidant activity of polysaccharide from spent Lentinus edodes substrate. Int. J. Biol. Macromol. 112: 976-984. https://doi.org/10.1016/j.ijbiomac.2018.01.196
  56. Wu S, Huang X. 2017. Preparation and antioxidant activities of oligosaccharides from Crassostrea gigas. Food Chem. 216: 243-246. https://doi.org/10.1016/j.foodchem.2016.08.043
  57. 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
  58. Min WH, Fang XB, Wu T, Fang L, Liu CL, Wang J. 2019. Characterization and antioxidant activity of an acidic exopolysaccharide from Lactobacillus plantarum JLAU103. J. Biosci. Bioeng. 127: 758-766. https://doi.org/10.1016/j.jbiosc.2018.12.004
  59. Liu CH, Wang CH, Xu ZL, Wang Y. 2007. Isolation, chemical characterization and antioxidant activities of two polysaccharides from the gel and the skin of Aloe barbadensis Miller irrigated with sea water. Process Biochem. 42: 961-970. https://doi.org/10.1016/j.procbio.2007.03.004
  60. Wang X, Shao C, Liu L, Guo X, Xu Y, Lv 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
  61. Fan J, Feng H, Yu Y, Sun M, Liu Y, Li T, et al. 2017. Antioxidant activities of the polysaccharides of Chuanminshen violaceum. Carbohydr. Polym. 157: 629-636. https://doi.org/10.1016/j.carbpol.2016.10.040
  62. Lin C, Wang C, Chang S, Inbaraj BS, Chen B. 2009. Antioxidative activity of polysaccharide fractions isolated from Lycium barbarum Linnaeus. Int. J. Biol. Macromol. 45: 146-151. https://doi.org/10.1016/j.ijbiomac.2009.04.014