Antioxidant and Probiotic Properties of Lactobacilli and Bifidobacteria of Human Origins

Abstract

Oxidative stress can cause various diseases including inflammation, neurological disorders, cancer, diabetes, and cardiovascular diseases. Due to the current search for natural antioxidants, probiotics have received increasing scientific interest and are facing a growing industrial demand. Although various strains of lactobacilli and bifidobacteria are currently used in numerous health food supplements, their antioxidative activities have been relatively poorly identified. Therefore, in this work, we evaluated the in vitro effect of antioxidative activities (through assays of 2,2-diphenyl-l-picrylhydrazyl (DPPH) and 2,2′-azinobis-(3-ethylbenzothiazorine-6-sulfonate) (ABTS) radical scavenging) and probiotic functional properties (cell viability in a simulated gastrointestinal tract, enzyme production, carbohydrate availability, and safely assessments) of Lactobacillus spp. and Bifidobacterium spp. isolated from human origins. From the nitric oxide (NO) assay screening, four strains (Bifidobacterium animalis subsp. lactis MG741, B. breve MG729, L. reuteri MG505, and L. rhamnosus MG316) were selected based on the yield amount of ferment productivity (> × 1010 CFU/g) and showed high antioxidant activities ranging from 22.2% to 38.2% in DPPH free radical scavenging, and 50.0% to 93.6% in ABTS radical scavenging. Regarding their functional properties as probiotics, these four strains were resistant to simulated gastric (pH 3 and 4) and intestinal fluids (pH 7 and 8), and showed potential for the promotion of health based on hemolysis, auto-aggregation, antibiotic susceptibility, enzyme production, and biochemical profiles. Altogether, our results showed that the selected probiotic strains may be good candidates as food ingredients to mitigate oxidative stress-related symptoms.

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References

  1. 1.

    Schieber, M. and N. S. Chandel, (2014) ROS function in redox signaling and oxidative stress. Curr. Biol. 24: R453–R462.

    CAS  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Mishra, V, C. Shah, N. Mokashe, R. Chavan, H. Yadav, and J. Prajapati, (2015) Probiotics as potential antioxidants: a systematic review. J. Agric. Food Chem. 63: 3615–3626.

    CAS  PubMed  Google Scholar 

  3. 3.

    Pizzino, G, N. Irrera, M. Cucinotta, G. Pallio, F. Mannino, V. Arcoraci, F. Squadrito, D. Altavilla, and A. Bitto, (2017) Oxidative stress: harms and benefits for human health. Oxid. Med. Cell Longer. 2017: 8416763.

    Google Scholar 

  4. 4.

    Higashi, Y., S. Sasaki, K. Nakagawa, H. Matsuura, T. Oshima, and K. Chayama, (2002) Endothelial function and oxidative stress in renovascular hypertension. New Engl. J. Med. 346: 1954–1962.

    CAS  PubMed  Google Scholar 

  5. 5.

    Ghiadoni, L., A. Magagna, D. Versari, I. Kardasz, Y. Huang, S. Taddei, and A. Salvetti, (2003) Different effect of antihypertensive drugs on conduit artery endothelial function. Hypertension. 41: 1281–1286.

    CAS  PubMed  Google Scholar 

  6. 6.

    Chisolm, G. M. and D. Steinberg, (2000) The oxidative modification hypothesis of atherogenesis: an overview. Free Radic. Biol. Med. 28: 1815–1826.

    CAS  PubMed  Google Scholar 

  7. 7.

    Zahavi, J., J. D. Betteridge, N. A. G. Jones, D. J. Galton, and V. V. Kakkar, (1981) Enhanced in vivo platelet release reaction and malondialdehyde formation in patients with hyperlipidemia. Am. J. Med. 70: 59–64.

    CAS  PubMed  Google Scholar 

  8. 8.

    Collier, A., A. Rumley, A. G. Rumley, J. R. Paterson, J. P. Leach, G. D. Lowe, and M. Small, (1992) Free radical activity and hemostatic factors in NIDDM patients with and without microalbuminuria. Diabetes. 41: 909–913.

    CAS  PubMed  Google Scholar 

  9. 9.

    Wang, D., D. A. Kreutzer, and J. M. Essigmann, (1998) Mutagenicity and repair of oxidative DNA damage: insights from studies using defined lesions. Mutat. Res. 400: 99–115.

    CAS  PubMed  Google Scholar 

  10. 10.

    Taysi, S., F. Polat, M. Gul, R. Sari, and E. Bakan, (2002) Lipid peroxidation, some extracellular antioxidants, and antioxidant enzymes in serum of patients with rheumatoid arthritis. Rheumatol. Int. 21:200–204.

    CAS  PubMed  Google Scholar 

  11. 11.

    Beal, M. F. (2002) Oxidatively modified proteins in aging and disease. Free Radical Bio. Med. 32: 797–803.

    CAS  Google Scholar 

  12. 12.

    Oliver, C. N., B. W. Ahn, E. J. Moerman, S. Goldstein, and E. R. Stadtman, (1987) Age-related changes in oxidized proteins. J. Biol. Chem. 262: 5488–5491.

    CAS  PubMed  Google Scholar 

  13. 13.

    Bodeker, G. and F. Kronenberg, (2002) A public health agenda for traditional, complementary, and alternative medicine. Am. J. Public Health. 92: 1582–1591.

    PubMed  PubMed Central  Google Scholar 

  14. 14.

    Luo, D. and B. Fang, (2008) Structural identification of ginseng polysaccharides and testing of their antioxidant activities. Carbohydr. Polym. 72: 376–381.

    CAS  Google Scholar 

  15. 15.

    Cai, Y, Q. Luo, M. Sun, and H. Corke, (2004) Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sci. 74: 2157–2184.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Fu, L., B. T. Xu, X. R. Xu, X. S. Qin, R. Y. Gan, and H. B. Li, (2010) Antioxidant capacities and total phenolic contents of 56 wild fruits from South China. Molecules. 15: 8602–8617.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Guo, Y. J., G. F. Deng, X. R. Xu, S. Wu, S. Li, E. Q. Xia, F. Li, F. Chen, W. H. Ling, and H. B. Li, (2012) Antioxidant capacities, phenolic compounds and polysaccharide contents of 49 edible macro-fungi. Food Fund. 3: 1195–1205.

    CAS  Google Scholar 

  18. 18.

    Li, Y, J. J. Zhang, D. P. Xu, T. Zhou, Y. Zhou, S. Li, and H. B. Li, (2016) Bioactivities and health benefits of wild fruits. Int. J. Mol. Sci. 17: 1258.

    PubMed Central  Google Scholar 

  19. 19.

    Choi, D. H., J. H. Han, K. H. Yu, M. Hong, S. Y. Lee, K. H. Park, S. U. Lee, and T. H. Kwon, (2020) Antioxidant and anti-obesity activities of Polygonum cuspidatum extract through alleviation of lipid accumulation on 3T3-L1 adipocytes. J. Microbiol. Biotechnol. 30: 21–30.

    PubMed  Google Scholar 

  20. 20.

    Ayyanna, R, D. Ankaiah, and V. Arul, (2018) Anti-inflammatory and antioxidant properties of probiotic bacterium Lactobacillus mucosae AN1 and Lactobacillus fermentum SNR1 in wistar albino rats. Front Microbiol. 9: 3063.

    PubMed  PubMed Central  Google Scholar 

  21. 21.

    Wang, Y, Y. Wu, Y. Wang, H. Xu, X. Mei, D. Yu, Y. Wang, and W. Li, (2017) Antioxidant properties of probiotic bacteria. Nutrients. 9: 521.

    PubMed Central  Google Scholar 

  22. 22.

    Tang, W, C. Li, Z. He, F. Pan, S. Pan, and Y. Wang, (2018) Probiotic properties and cellular antioxidant activity of Lactobacillus plantarum MA2 isolated from Tibetan kefir grains. Probiotics Antimicro. Proteins. 10: 523–533.

    CAS  Google Scholar 

  23. 23.

    Bernini, L. I., A. N. C. Simao, C. H. B. de Souza, D. F. Alfieri, L. G. Segura, G. N. Costa, and I. Dichi, (2018) Effect of Bifidobacterium lactis HNO 19 on inflammatory markers and oxidative stress in subjects with and without the metabolic syndrome. Br. J. Nutr. 120: 645–652.

    CAS  PubMed  Google Scholar 

  24. 24.

    Kang, C. H., S. H. Han, J. S. Kim, Y. Kim, Y. Jeong, H. M. Park, N. S. Paek, (2019) Inhibition of nitric oxide production, oxidative stress prevention, and probiotic activity of lactic acid bacteria isolated from the human vagina and fermented food. Microorganisms. 7: 109.

    CAS  PubMed Central  Google Scholar 

  25. 25.

    Korhonen, R, R. Korpela, M. Saxelin, M. Mäki, H. Kankaanranta, and E. Moilanen, (2001) Induction of nitric oxide synthesis by probiotic Lactobacillus rhamnosus GG in J774 macrophages and human T84 intestinal epithelial cells. Inflammation. 25: 223–232.

    CAS  PubMed  Google Scholar 

  26. 26.

    Oh, N. S., J. Y. Joung, J. Y. Lee, and Y. Kim, (2018) Probiotic and anti-inflammatory potential of Lactobacillus rhamnosus 4B15 and Lactobacillus gasseri 4M13 isolated from infant feces. PLoS One. 13:e0192021.

    PubMed  PubMed Central  Google Scholar 

  27. 27.

    Yu, H. S., N. K. Lee, A. J. Choi, J. S. Choe, C. H. Bae, and H. D. Paik, (2019) Anti-inflammatory potential of probiotic strain Weissella cibaria JW15 isolated from Kimchi through regulation of NF-kappaB and MAPKs pathways in LPS-induced RAW 264.7 cells. J. Microbiol. Biotechnol. 29: 1022–1032.

    CAS  PubMed  Google Scholar 

  28. 28.

    Song, M. W, H. J. Jang, K. T. Kim, and H. D. Paik, (2019) Probiotic and antioxidant properties of novel Lactobacillus brevis KCCM 12203P isolated from Kimchi and evaluation of immune-stimulating activities of Its heat-killed cells in RAW 264.7 cells. J. Microbiol. Biotechnol. 29: 1894–1903.

    PubMed  Google Scholar 

  29. 29.

    Fenster, K., B. Freeburg, C. Hollard, C. Wong, R. R. Laursen, and A. C. Ouwehand, (2019) The production and delivery of probiotics: A review of a practical approach. Microorganisms. 7: 83.

    CAS  PubMed Central  Google Scholar 

  30. 30.

    Amaretti, A., M. di Nunzio, A. Pompei, S. Raimondi, M. Rossi, and A. Bordoni, (2013) Antioxidant properties of potentially probiotic bacteria: in vitro and in vivo activities. Appl. Microbiol. Biotechnol. 97: 809–817.

    CAS  PubMed  Google Scholar 

  31. 31.

    Delgado, S., A. M. O. Leite, P. Ruas-Madiedo, and B. Mayo, (2015) Probiotic and technological properties of Lactobacillus spp. strains from the human stomach in the search for potential candidates against gastric microbial dysbiosis. Front. Microbiol. 5: 766.

    PubMed  PubMed Central  Google Scholar 

  32. 32.

    Ouwehand, A. C, S. Salminen, and E. Isolauri, (2002) Probiotics: an overview of beneficial effects. Proceedings of the seventh Symposium on lactic acid bacteria: genetics, metabolism and applications. September 1–5. Egmond aan Zee, Netherlands.

    Google Scholar 

  33. 33.

    Lee, Y. K. and S. Salminen, (1995) The coming of age of probiotics. Trends Food Sci. Technol. 6: 241–245.

    Google Scholar 

  34. 34.

    Chang, C. E., S. I. Pavlova, L. Tao, E. K. Kim, S. C. Kim, H. S. Yun, and J. S. So, (2002) Molecular identification of vaginal Lactobacillus spp. isolated from Korean women. J. Microbiol. Biotechnol. 12: 312–317.

    CAS  Google Scholar 

  35. 35.

    Lyons, C. R, G. I. Orloff, and I. M. Cunningham, (1992) Molecular cloning and functional expression of an inducible nitric oxide synthase from a murine macrophage cell line. J. Biol. Chem. 267: 6370–6374.

    CAS  PubMed  Google Scholar 

  36. 36.

    Blois, M. S. (1958) Antioxidant determinations by the use of a stable free radical. Nature. 181: 1199–1200.

    CAS  Google Scholar 

  37. 37.

    Re, R, N. Pellegrini, A. Proteggente, A. Pannala, M. Yang, and C. Rice-Evans (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med. 26: 1231–1237.

    CAS  PubMed  Google Scholar 

  38. 38.

    Maragkoudakis, P. A., G. Zoumpopoulou, C. Miaris, G. Kalantzopoulos, B. Pot, and E. Tsakalidou, (2006) Probiotic potential of Lactobacillus strains isolated from dairy products. Int. Dairy 1 16: 189–199.

    CAS  Google Scholar 

  39. 39.

    Kos, B., J. Suskovic, S. Vukovic, M. Simpraga, J. Frece, and S. Matosic, (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J. Appl. Microbiol. 94: 981–987.

    CAS  PubMed  Google Scholar 

  40. 40.

    EFSA (2012) Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA J. 10: 2740.

    Google Scholar 

  41. 41.

    Squadrito, G. L. and W. A. Pryor, (1995) The formation of peroxynitrite in vivo from nitric oxide and superoxide. Chem Biol Interact. 96: 203–206.

    CAS  PubMed  Google Scholar 

  42. 42.

    Li, S., Y. Zhao, L. Zhang, X. Zhang, L. Huang, D. Li, C. Niu, Z. Yang, and Q. Wang, (2012) Antioxidant activity of Lactobacillus plantarum strains isolated from traditional Chinese fermented foods. Food Chem. 135: 1914–1919.

    CAS  PubMed  Google Scholar 

  43. 43.

    Afify, A. E. M. M., R. M. Romeilah, S. I. Sultan, and M. M. Hussein, (2012) Antioxidant activity and biological evaluations of probiotic bacteria strains. Int. J. Acad. Res. 4: 131–139.

    Google Scholar 

  44. 44.

    Lin, M. Y. and C. L. Yen, (1999) Inhibition of lipid peroxidation by Lactobacillus acidophilus and Bifidobacterium longum.J. Agric. Food Chem. 47: 3661–3664.

    CAS  PubMed  Google Scholar 

  45. 45.

    Kim, I. Y, S. I. Choi, and T. R. Heo, (2003) Screening of antioxidative activity of Bifidobacterium species isolated from Korean infant feces and their identification. Biotechnol. Bioprocess Eng 8: 199–204.

    CAS  Google Scholar 

  46. 46.

    Di Cerbo, A., B. Palmieri, M. Aponte, J. C. Morales-Medina, and T. Iannitti, (2016) Mechanisms and therapeutic effectiveness of lactobacilli. J. Clin. Pathol. 69: 187–203.

    CAS  PubMed  Google Scholar 

  47. 47.

    Ross, R. P., C. Desmond, G. F. Fitzgerald, and C. Stanton, (2005) Overcoming the technological hurdles in the development of probiotic foods. J. Appl. Microbiol. 98: 1410–1417.

    CAS  PubMed  Google Scholar 

  48. 48.

    Morelli, L. (2007) In vitro assessment of probiotic bacteria: from survival to functionality. Int. Dairy J. 17: 1278–1283.

    Google Scholar 

  49. 49.

    Liu, I, S. H. I. Chan, I. Chen, C. Solem, and P. R. Jensen, (2019) Systems Biology-A guide for understanding and developing improved strains of lactic acid bacteria. Front. Microbiol. 10: 876.

    PubMed  PubMed Central  Google Scholar 

  50. 50.

    Nguyen, T. H., Y. Kim, I. S. Kim, Y. Jeong, H. M. Park, I. W. Kim, I. E. Kim, H. Kim, N. S. Paek, and C. H. Kang, (2020) Evaluating the cryoprotective encapsulation of the lactic acid bacteria in simulated gastrointestinal conditions. Biotechnol. Bioprocess Eng. 25: 287–292.

    CAS  Google Scholar 

  51. 51.

    Garcia-Cayuela, T, A. M. Korany, I. Bustos, L. P. G. de Cadinanos, T. Requena, C. Peláez C, and M. C. Martinez-Cuestaa (2014) Adhesion abilities of dairy Lactobacillus plantarum strains showing an aggregation phenotype. Food Res. Int. 57: 44–50.

    CAS  Google Scholar 

  52. 52.

    Bouchard, D. S., B. Seridan, T. Saraoui, L. Rault, P. Germon, C. Gonzalez-Moreno, F. M. E. Nader-Macias, D. Baud, P. François, V. Chuat, F. Chain, P. Langella, J. Nicoli, Y. Le Loir, and S. Even, (2015) Lactic acid bacteria isolated from bovine mammary microbiota: potential allies against bovine mastitis. PLoS One. 10:e0144831.

    PubMed  PubMed Central  Google Scholar 

  53. 53.

    Ramos, C. L., L. Thorsen, R. F. Schwan, and L. Jespersen, (2013) Strain-specific probiotics properties of Lactobacillus fermentum, Lactobacillus plantarum and Lactobacillus brevis isolates from Brazilian food products. Food Microbiol. 36: 22–29.

    CAS  PubMed  Google Scholar 

  54. 54.

    Li, Q., X. Liu, M. Dong, I. Zhou, and Y. Wang, (2015) Aggregation and adhesion abilities of 18 lactic acid bacteria strains isolated from traditional fermented food. Int. J. Agric. Pol. Res. 3: 84–92.

    Google Scholar 

  55. 55.

    Pessoa, W. F. B., A. C. C. Melgaço, M. E. de Almeida, L. P. Ramos, R. P. Rezende, and C. C. Romano, (2017) In vitro activity of lactobacilli with probiotic potential isolated from cocoa fermentation against gardnerella vaginalis. Biomed Res. Int. 2017: 3264194.

    PubMed  PubMed Central  Google Scholar 

  56. 56.

    Charteris, W. P., P. M. Kelly, L. Morelli, and I. K. Collins, (2001) Gradient diffusion antibiotic susceptibility testing of potentially probiotic lactobacilli. J. Food Prot. 64: 2007–2014.

    CAS  PubMed  Google Scholar 

  57. 57.

    Imperial, I. C. V. I. and I A. Ibana, (2016) Addressing the antibiotic resistance problem with probiotics: reducing the risk of its double-edged sword effect. Front. Microbiol. 7: 1983.

    PubMed  PubMed Central  Google Scholar 

  58. 58.

    George, J. (2008) Elevated serum ß-glucuronidase reflects hepatic lysosomal fragility following toxic liver injury in rats. Biochem. Cell Biol. 86:235–243.

    CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Professor Nam Soo, Han (Chungbuk University) for contributing to the NO assay screening.

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Correspondence to Chang-Ho Kang.

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Kim, H., Kim, J., Kim, Y. et al. Antioxidant and Probiotic Properties of Lactobacilli and Bifidobacteria of Human Origins. Biotechnol Bioproc E 25, 421–430 (2020). https://doi.org/10.1007/s12257-020-0147-x

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Keywords

  • nitric oxide
  • antioxidant
  • probiotics
  • Lactobacillus
  • Bifidobacterium