Advertisement

Characterization, the Antioxidant and Antimicrobial Activity of Exopolysaccharide Isolated from Poultry Origin Lactobacilli

  • Muhammad Shahid Riaz Rajoka
  • Hafiza Mahreen Mehwish
  • Hafiz Fakhar Hayat
  • Nazim Hussain
  • Sobia Sarwar
  • Humaira Aslam
  • Ahmad Nadeem
  • Junling Shi
Article
  • 29 Downloads

Abstract

The natural antioxidant agent is urgently needed to prevent the negative effects of newly generated free radicals and chronic disorders. Recently, the microbial exopolysaccharide (EPS) is currently used as a potential biopolymer due to its unique biological characteristics. In this study, the biological potential was carried out on the EPSs produced by Lactobacillus reuteri SHA101 (EPS-lr) and Lactobacillus vaginalis SHA110 (EPS-lvg) isolated from gut cecum samples of healthy poultry birds (hen). As results, the EPS-lr and EPS-lvg showed the emulsifying activity of 37.8 ± 1.6% and 27.8 ± 0.5% after the 360 h, respectively. The scanning electron microscopy analysis of EPS-lr and EPS-lvg demonstrated a smooth surface with a compact structure. The both EPSs exhibited strong antibacterial activity against E. coli and Salmonella typhimurium in vitro. In additions, at 4 mg/mL concentration, the EPS-lr and EPS-lvg samples showed potent antioxidant activity regarding hydroxyl radical DPPH (2,2-diphenyl-1-picrylhydrazyl) radical, superoxide anion radical and reducing power at OD700 nm. Furthermore, the EPS-lr and EPS-lvg (600 μg/mL) possessed antitumor activity against colon cancer (Caco-2) cell after 72 h. The results suggested that these EPSs would have great potential in the application of antitumor and antioxidant foods, biomedicine, and pharmaceutics.

Keywords

Lactobacillus reuteri Lactobacillus vaginalis Poultry birds Exopolysaccharide Antioxidant Anticancer 

Notes

Funding Information

This study was supported by the National Key Technology R&D Program (grant number 2015BAD16B02) and the National Natural Science Foundation of China (NSFC) (grant numbers 31201408 and 31471718).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that there are no conflicts of interests.

References

  1. 1.
    Kanmani P, Satish kR, Yuvaraj N, Paari KA, Pattukumar V, Arul V (2011) Production and purification of a novel exopolysaccharide from lactic acid bacterium Streptococcus phocae PI80 and its functional characteristics activity in vitro. Bioresour Technol 102(7):4827–4833.  https://doi.org/10.1016/j.biortech.2010.12.118 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Liu C, Lu J, Lu L, Liu Y, Wang F, Xiao M (2010) Isolation, structural characterization and immunological activity of an exopolysaccharide produced by Bacillus licheniformis 8-37-0-1. Bioresour Technol 101(14):5528–5533.  https://doi.org/10.1016/j.biortech.2010.01.151 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Kavita K, Singh VK, Mishra A, Jha B (2014) Characterisation and anti-biofilm activity of extracellular polymeric substances from Oceanobacillus iheyensis. Carbohydr Polym 101(1):29–35.  https://doi.org/10.1016/j.carbpol.2013.08.099 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Ismail B, Nampoothiri KM (2010) Production, purification and structural characterization of an exopolysaccharide produced by a probiotic Lactobacillus plantarum MTCC 9510. Arch Microbiol 192(12):1049–1057.  https://doi.org/10.1007/s00203-010-0636-y CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Li S, Huang R, Shah NP, Tao X, Xiong Y, Wei H (2014) Antioxidant and antibacterial activities of exopolysaccharides from Bifidobacterium bifidum WBIN03 and Lactobacillus plantarum R315. J Dairy Sci 97(12):7334–7343.  https://doi.org/10.3168/jds.2014-7912 CrossRefGoogle Scholar
  6. 6.
    Kanmani P, Suganya K, Kumar RS, Yuvaraj N, Pattukumar V, Paari KA, Arul V (2013) Synthesis and functional characterization of antibiofilm exopolysaccharide produced by Enterococcus faecium MC13 isolated from the gut of fish. Appl Biochem Biotechnol 169(3):1001–1015.  https://doi.org/10.1007/s12010-012-0074-1 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Patten DA, Leivers S, Chadha MJ, Maqsood M, Humphreys PN, Laws AP, Collett A (2013) The structure and immunomodulatory activity on intestinal epithelial cells of the EPSs isolated from Lactobacillus helveticus sp. rosyjski and Lactobacillus acidophilus sp. 5e2. Carbohydr Res 384C(1):119–127.  https://doi.org/10.1016/j.carres.2013.12.008. CrossRefGoogle Scholar
  8. 8.
    Landersjö C, Yang Z, Huttunen E, Widmalm G (2002) Structural studies of the exopolysaccharide produced by Lactobacillus rhamnosus strain GG (ATCC 53103). Biomacromolecules 3(4):880–884CrossRefGoogle Scholar
  9. 9.
    Péant B, Lapointe G, Gilbert C, Atlan D, Ward P, Roy D (2005) Comparative analysis of the exopolysaccharide biosynthesis gene clusters from four strains of Lactobacillus rhamnosus. Microbiology 151(6):1839–1851CrossRefGoogle Scholar
  10. 10.
    Bjarnsholt T (2013) The role of bacterial biofilms in chronic infections. Apmis Suppl 136:1–51.  https://doi.org/10.1111/apm.12099 CrossRefGoogle Scholar
  11. 11.
    Zhang Z, Liu Z, Tao X, Wei H (2016) Characterization and sulfated modification of an exopolysaccharide from Lactobacillus plantarum ZDY2013 and its biological activities. Carbohydr Polym 153:25–33.  https://doi.org/10.1016/j.carbpol.2016.07.084 CrossRefGoogle Scholar
  12. 12.
    Li W, Ji J, Chen X, Jiang M, Rui X, Dong M (2014) Structural elucidation and antioxidant activities of exopolysaccharides from Lactobacillus helveticus MB2-1. Carbohydr Polym 102(1):351–359.  https://doi.org/10.1016/j.carbpol.2013.11.053 CrossRefGoogle Scholar
  13. 13.
    Rajoka MSR, Hayat HF, Sarwar S, Mehwish HM, Ahmad F, Hussain N, Shah SZH, Khurshid M, Siddiqu M, Shi J (2018) Isolation and evaluation of probiotic potential of lactic acid bacteria isolated from poultry intestine. Microbiol 87(1):116–126.  https://doi.org/10.1134/s0026261718010150 CrossRefGoogle Scholar
  14. 14.
    Wang K, Li W, Rui X, Chen X, Jiang M, Dong M (2014) Structural characterization and bioactivity of released exopolysaccharides from Lactobacillus plantarum 70810. Int J Biol Macromol 67(6):71–78.  https://doi.org/10.1016/j.ijbiomac.2014.02.056 CrossRefGoogle Scholar
  15. 15.
    Xu R, Shen Q, Ding X, Gao W, Li P (2011) Chemical characterization and antioxidant activity of an exopolysaccharide fraction isolated from Bifidobacterium animalis RH. Eur Food Res Technol 232(2):231–240.  https://doi.org/10.1007/s00217-010-1382-8 CrossRefGoogle Scholar
  16. 16.
    Chen R, Meng F, Liu Z, Chen R, Zhang M (2010) Antitumor activities of different fractions of polysaccharide purified from Ornithogalum caudatum ait. Carbohydr Polym 80(3):845–851.  https://doi.org/10.1016/j.carbpol.2009.12.042 CrossRefGoogle Scholar
  17. 17.
    Qin X, Zhang M, Wu L (2012) Purification and characterization of Cu,Zn superoxide dismutase from pumpkin (Cucurbita moschata) pulp. Eur Food Res Technol 235(6):1049–1054.  https://doi.org/10.1007/s00217-012-1829-1 CrossRefGoogle Scholar
  18. 18.
    Sasikumar K, Kozhummal Vaikkath D, 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 CrossRefGoogle Scholar
  19. 19.
    Anjum, Nomana, Ahmed, Zaheer, Ahmad, Asif, Khan, Tariq S (2013) Characterization of exopolysaccharide produced by Lactobacillus kefiranofaciens ZW3 isolated from Tibet kefir - part II. Food Hydrocoll 30 (1):343–350.  https://doi.org/10.1016/j.foodhyd.2012.06.009 CrossRefGoogle Scholar
  20. 20.
    Qiao D, Ke C, Hu B, Luo J, Ye H, Sun Y, Yan X, Zeng X (2009) Antioxidant activities of polysaccharides from Hyriopsis cumingii. Carbohydr Polym 78(2):199–204.  https://doi.org/10.1016/j.carbpol.2009.03.018 CrossRefGoogle Scholar
  21. 21.
    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(2):275–281.  https://doi.org/10.1016/j.carbpol.2009.03.046 CrossRefGoogle Scholar
  22. 22.
    Fontana C, Cocconcelli PS, Vignolo G, Saavedra L (2015) Occurrence of antilisterial structural bacteriocins genes in meat borne lactic acid bacteria. Food Control 47:53–59.  https://doi.org/10.1016/j.foodcont.2014.06.021 CrossRefGoogle Scholar
  23. 23.
    Aaltonen J, Ojala T, Laitinen K, Poussa T, Ozanne S, Isolauri E (2011) Impact of maternal diet during pregnancy and breastfeeding on infant metabolic programming: a prospective randomized controlled study. Eur J Clin Nutr 65(1):10–19CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Tsai Y-T, Cheng P-C, Pan T-M (2012) The immunomodulatory effects of lactic acid bacteria for improving immune functions and benefits. Appl Microbiol Biotechnol 96(4):853–862.  https://doi.org/10.1007/s00253-012-4407-3 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    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(3):895–903.  https://doi.org/10.1016/j.carbpol.2010.06.013 CrossRefGoogle Scholar
  26. 26.
    Yang ZN, Li SY, Zhang X, Zeng XP, Li D, Zhao YJ, Zhang J (2010) Capsular and slime-polysaccharide production by Lactobacillus rhamnosus JAAS8 isolated from Chinese sauerkraut: potential application in fermented milk products. J Biosci Bioeng 110(1):53–57.  https://doi.org/10.1016/j.jbiosc.2009.12.010 CrossRefGoogle Scholar
  27. 27.
    Costa NE, Wang L, Auty ME, Hannon JA, McSweeney PLH, Beresford TP (2012) Rheological, microscopic and primary chemical characterisation of the exopolysaccharide produced by Lactococcus lactis subsp. cremoris DPC6532. Dairy Sci Technol 92(3):219–235.  https://doi.org/10.1007/s13594-012-0059-4 CrossRefGoogle Scholar
  28. 28.
    Juditha P, Marianol DLC, Analíag A (2008) Gelling properties of kefiran, a food-grade polysaccharide obtained from kefir grain. Food Hydrocoll 22(8):1520–1527.  https://doi.org/10.1016/j.foodhyd.2007.10.005 CrossRefGoogle Scholar
  29. 29.
    Ale EC, Perezlindo MJ, Burns P, Tabacman E, Reinheimer JA, Binetti AG (2016) Exopolysaccharide from Lactobacillus fermentum Lf2 and its functional characterization as a yogurt additive. J dairy Res 83(4):487–492.  https://doi.org/10.1017/s0022029916000571 CrossRefGoogle Scholar
  30. 30.
    Willumsen PA, Karlson U (1996) Screening of bacteria, isolated from PAH-contaminated soils, for production of biosurfactants and bioemulsifiers. Biodegradation 7(5):415–423CrossRefGoogle Scholar
  31. 31.
    Devi PB, Kavitake D, Shetty PH (2016) Physico-chemical characterization of galactan exopolysaccharide produced by Weissella confusa KR780676. Int J Biol Macromol 93 (Pt A) 93:822–828.  https://doi.org/10.1016/j.ijbiomac.2016.09.054 CrossRefGoogle Scholar
  32. 32.
    Riaz Rajoka MS, Jin M, Haobin Z, Li Q, Shao D, Jiang C, Huang Q, Yang H, Shi J, Hussain N (2018) Functional characterization and biotechnological potential of exopolysaccharide produced by Lactobacillus rhamnosus strains isolated from human breast milk. LWT-Food sci Technol 89:638–647.  https://doi.org/10.1016/j.lwt.2017.11.034 CrossRefGoogle Scholar
  33. 33.
    Zhu KX, Sheng H, Wei P, Qian HF, Zhou HM (2010) Effect of ultrafine grinding on hydration and antioxidant properties of wheat bran dietary fiber. Food Res Int 43(4):943–948.  https://doi.org/10.1016/j.foodres.2010.01.005 CrossRefGoogle Scholar
  34. 34.
    Wang K, Li W, Rui X, Li T, Chen X, Jiang M, Dong M (2015) Chemical modification, characterization and bioactivity of a released exopolysaccharide (r-EPS1) from Lactobacillus plantarum 70810. Glycoconj J 32(1):1–11.  https://doi.org/10.1007/s10719-014-9567-1. CrossRefGoogle Scholar
  35. 35.
    Huang SQ, Ding S, Fan L (2012) Antioxidant activities of five polysaccharides from Inonotus obliquus. Int J Biol Macromol 50(5):1183–1187.  https://doi.org/10.1016/j.ijbiomac.2012.03.019 CrossRefGoogle Scholar
  36. 36.
    Tokura S, Ueno K, Miyazaki S, Nishi N (1996) Molecular weight dependent antimicrobial activity by chitosan. Macromol Symp 120(1):1–9CrossRefGoogle Scholar
  37. 37.
    Li J, Wu Y, Zhao L (2016) Antibacterial activity and mechanism of chitosan with ultra high molecular weight. Carbohydr Polym 148:200–205.  https://doi.org/10.1016/j.carbpol.2016.04.025 CrossRefGoogle Scholar
  38. 38.
    Maalej H, Boisset C, Hmidet N, Colinmorel P, Buon L, Nasri M (2017) Depolymerization of Pseudomonas stutzeri exopolysaccharide upon fermentation as a promising production process of antibacterial compounds. Food Chem 227:22–32.  https://doi.org/10.1016/j.foodchem.2017.01.079. CrossRefGoogle Scholar
  39. 39.
    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 CrossRefGoogle Scholar
  40. 40.
    Kim Y, Oh S, Yun HS, Oh S, Kim SH (2010) Cell-bound exopolysaccharide from probiotic bacteria induces autophagic cell death of tumour cells. Lett Appl Microbiol 51(2):123–130.  https://doi.org/10.1111/j.1472-765X.2010.02859.x. CrossRefPubMedGoogle Scholar
  41. 41.
    Li W, Tang W, Ji J, Xia X, Rui X, Chen X, Jiang M, Zhou J, Dong M (2015) Characterization of a novel polysaccharide with anti-colon cancer activity from Lactobacillus helveticus MB2-1. Carbohydr Res 411:6–14.  https://doi.org/10.1016/j.carres.2014.12.014 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Food Science and Engineering, College of Chemistry and Chemical EngineeringShenzhen UniversityShenzhenPeople’s Republic of China
  2. 2.Key Laboratory for Space Bioscience and Space Biotechnology, School of Life SciencesNorthwestern Polytechnical UniversityXi’anPeople’s Republic of China
  3. 3.Department of Pharmacy, School of Medicine, Key Laboratory of Novel Health Care Product, Engineering Laboratory of Shenzhen Natural Small Molecules Innovative DrugsShenzhen UniversityShenzhenPeople’s Republic of China
  4. 4.Institute of MicrobiologyUniversity of AgricultureFaisalabadPakistan
  5. 5.Center for Applied Molecular BiologyUniversity of PunjabLahorePakistan
  6. 6.Department of PharmacyUniversity of AgricultureFaisalabadPakistan
  7. 7.Muhammad Medical CollegeMirpur KhasPakistan
  8. 8.Nuclear Institute for Agriculture and BiologyFaisalabadPakistan

Personalised recommendations