Health promoting benefits of postbiotics produced by lactic acid bacteria: Exopolysaccharide

Abstract

Exopolysaccharides are high molecular weight polymers of repeated sugar units with diverse chemical structure and unique properties and produced by microorganisms. Lactic acid bacteria are important exopolysaccharide producers. Lactic acid bacteria derived exopolysaccharides, one of the postbiotics, are known to have technological properties such as stabilizing, thickening, emulsifing and also biological activities. Lactic acid bacteria can synthesis exopolysaccharides with large structural variability and this diversity brings these polymers to possess several bioactivities. Bioactivities such as immunomodulatory, antiinflammatory, antitumor and antimutagenicity, antioxidant, antibacterial and antiviral, cholesterol-lowering, antihypertensive activity and gastro-protective activity bring these biopolymers commercial value in the global market and potential to be used in biomedical and pharmaceutical applications. Therefore, to evaluate the availability of these natural exopolysaccharides for new applications extensive understanding of the structure-function relationships will be required. In this review, it is presented a comprehensive overview for the most recent reports on the health benefits of postbiotic lactic acid bacterial exopolysaccharides.

Keywords

• Lactic acid bacteria
• Exopolysaccharides
• Bioactivities

References

1. Abbasi, A., Rad, A. H., Ghasempour, Z., Sabahi, S., Kafil, H. S., Hasannezhad, P., Saadat, Y. R., & Shahbazi, N. (2021). The biological activities of postbiotics in gastrointestinal disorders. Critical Reviews in Food Science and Nutrition, 1-22. https:// doi.org/10.1080/10408398.2021.1895061
2. Adebayo-Tayo, B., & Fashogbon, R. (2020). In vitro antioxidant, antibacterial, in vivo immunomodulatory, antitumor and hematological potential of exopolysaccharide produced by wild type and mutant Lactobacillus delbureckii subsp.bulgaricus. Heliyon, 6(2), 1-10. https://doi.org/10.1016/j.heliyon.2020.e03268
3. Adebayo-Tayo, B., Ishola, R., & Oyewunmi, T. (2018). Characterization, antioxidant and immunomodulatory potential on exopolysaccharide produced by wild type and mutant Weissella confusa strains. Biotechnology Reports, 19, e00271. https://doi.org/10.1016/j.btre.2018.e00271
4. Adesulu-Dahunsi, A. T., Sanni, A. I., Jeyaram, K., Ojediran, J. O., Ogunsakin, A. O., & Banwo, K. (2018). Extracellular polysaccharide from Weissella confusa OF126: Production, optimization, and characterization. International Journal of Biological Macromolecules, 111, 514-525. https://doi.org/10.1016/j.ijbiomac.2018.01.060
5. Alsaadi, L. G., Baker, B. A. A., Kadhem, B. M., Mahdi, L. H., & Mater, H. N. (2020). Exopolysaccharide as antiviral, antimicrobial and as immunostimulants: A review. Plant Archives, 20(2), 5859-5875. eISSN: 2581-6063.
6. Angelin, J., & Kavitha, M. (2020). Exopolysaccharides from probiotic bacteria and their health potential. International Journal of Biological Macromolecules, 162, 853-865. https://doi.org/10.1016/j.ijbiomac.2020.06.190
7. Buddana, S. K., Venkata Naga Varanasi, Y., & Reddy Shetty, P. (2015). Fibrinolytic, antiinflammatory and antimicrobial properties of α-(1-3)-glucans produced from Streptococcus mutans (MTCC 497). Carbohydrate Polymers, 15, 152–159. https://doi.org/10.1016/j.carbpol.2014.08.083
8. Castro-Bravo, N., Wells, J. M., Margolles, A., & Ruas-Madiedo, P. (2018). Interactions of surface exopolysaccharides from Bifidobacterium and Lactobacillus within the intestinal environment. Front in Microbiology, 9, 2426, 1-15. https://doi.org/10.3389/fmicb.2018.02426

9. Chaisuwan, W., Jantanasakulwong, K., Wangtueai, S., Phimolsiripol, Y., Chaiyaso, T., Techapun, C., Phongthai, S., You, S., Regenstein, J. M., & Seesuriyachan, P. (2020). Microbial exopolysaccharides for immune enhancement: Fermentation, modifications and bioactivities, Food Bioscience, 35, 1-17. https://doi.org/10.1016/j.fbio.2020.100564
10. Chen, Y. C., Wu, Y. J., & Hu, C. Y. (2019). Monosaccharide composition influence and immunomodulatory effects of probiotic exopolysaccharides. International Journal of Biological Macromolecules, 133, 575-582. https://doi.org/10.1016/j.ijbiomac.2019.04.109
11. Chien, Y. L., Wu, L. Y., Lee, T. C., & Hwang, L. S. (2010). Cholesterol-lowering effect of phytosterol-containing lactic-fermented milk powder in hamsters. Food Chemistry, 119(3), 1121-1126. https://doi.org/10.1016/j.foodchem.2009.08.023
12. Deepak, V., Ram Kumar Pandian, S., Sivasubramaniam, S. D., Nellaiah, H., & Sundar, K. (2016a). Optimization of anticancer exopolysaccharide production from probiotic Lactobacillus acidophilus by response surface methodology. Preparative Biochemistry 396 and Biotechnology, 46(3), 288–297. https://doi.org/10.1080/10826068.2015.1031386
13. Deepak, V., Ramachandran, S., Balahmar, R. M., Pandian, S. R. K., Sivasubramaniam, S. D., Nellaiah, H., & Sundar, K. (2016b). In vitro evaluation of anticancer properties of exopolysaccharides from Lactobacillus acidophilus in colon cancer cell lines. In Vitro Cellular &Developmental Biology-Animal, 52(2),163-173. https://doi.org/10.1007/s11626-015-9970-3
14. Dilna, S. V., Surya, H., Aswathy, R. G., Varsha, K. K., Sakthikumar, D. N., Pandey, A., Nampoothiri, K. M. (2015). Characterization of an exopolysaccharide with potential 404 health-benefit properties from a probiotic Lactobacillus plantarum RJF4. LWT-Food Science and Technology, 64, 1179-1186. https://doi.org/10.1016/j.lwt.2015.07.040
15. Dinarello, C. A. (2000). Proinflammatory cytokines. Chest, 118(2), 503–508. https://doi.org/10.1378/chest.118.2.503
16. Farag, M. M., Moghannem, S. A., Shehabeldine, A. M., & Azab, M. S. (2020). Antitumor effect of exopolysaccharide produced by Bacillus mycoides. Microbial pathogenesis, 140, 1-10. https://doi.org/10.1016/j.micpath.2019.103947
17. Furuno, T., & Nakanishi, M. (2012). Kefiran suppresses antigen-induced mast cell activation. Biological and Pharmaceutical Bulletin, 35(2), 178–183. https://doi.org/10.1248/bpb.35.178
18. Glass, C. K. & Witztum, J. L. (2001). Atherosclerosis: the road ahead. Cell, 104(4), 503-516. https://doi.org/10.1016/s0092-8674(01)00238-0
19. Hasheminya, S. M., & Dehghannya, J. (2020). Novel ultrasound-assisted extraction of kefiran biomaterial, a prebiotic exopolysaccharide, and investigation of its physicochemical, antioxidant and antimicrobial properties. Materials Chemistry and Physics, 243, 1-8. https://doi.org/ 10.1016/j.matchemphys.2020.122645
20. Ismail, B., & Nampoothiri, K.M. (2013). Exposition of antitumour activity of a chemically characterized exopolysaccharide from a probiotic Lactobacillus plantarum MTCC 9510. Biologia, 68(6), 1041–1047. https://doi.org/10.2478/s11756-013-0275-2
21. Jurášková, D., Ribeiro, S. C., & Silva, C. C. (2022). Exopolysaccharides produced by lactic acid bacteria: From biosynthesis to health-promoting properties, Foods, 11(2), 156. https://doi.org/10.3390/foods11020156
22. Jeong, D., Kim, D. H., Kang, I. B., Kim, H., Song, K. Y., Kim, H. S., & Seo, K. H. (2017). Characterization and antibacterial activity of a novel exopolysaccharide produced by Lactobacillus kefiranofaciens DN1 isolated from kefir. Food Control, 78, 436-442. https://doi.org/10.1016/j.foodcont.2017.02.033
23. Kavitake, D., Kalahasti, K. K., Devi, P. B., Ravi, R., & Shetty, P. H. (2020). Galactan exopolysaccharide based flavour emulsions and their application in improving the texture and sensorial properties of muffin. Bioactive Carbohydrates and Dietary Fibre, 24, 1-8. https://doi.org/10.1016/j.bcdf.2020.100248
24. Khalil, E. S., Abd Manap, M. Y., Mustafa, S., Alhelli, A. M., & Shokryazdan, P. (2018). Probiotic properties of exopolysaccharide-producing lactobacillus strains ısolated from Tempoyak. Molecules, 23(2), 398, 1-20. https://doi.org/10.3390/molecules23020398
25. Kim, K., Lee, G., Thanh, H. D., Kim, J. H., Konkit, M., Yoon, S., Park, M., Yang, S., Park, E., & Kim, W. (2018). Exopolysaccharide from Lactobacillus plantarum LRCC5310 offers protection against rotavirus-induced diarrhea and regulates inflammatory response. Journal of Dairy Science, 101(7), 5702-5712. https://doi.org/10.3168/jds.2017-14151
26. Korcz, E., Kerényi, Z., & Varga, L. (2018). Dietary fibers, prebiotics, and exopolysaccharides produced by lactic acid bacteria: potential health benefits with special regard to cholesterol-lowering effects. Food & Function, 9(6), 3057-3068. https://doi.org/10.1039/c8fo00118a
27. Kšonžeková, P., Bystrický, P., Vlčková, S., Pätoprstý, V., Pulzová, L., Mudroňová, D., Kubašková, T., Csank, T., & Tkáčiková, Ľ. (2016). Exopolysaccharides of Lactobacillus reuteri: Their influence on adherence of E. coli to epithelial cells and inflammatory response. Carbohydrate Polymers, 141, 10-19. https://doi.org/10.1016/j.carbpol.2015.12.037
28. Kumar, R., Bansal, P., Singh, J., & Dhanda, S. (2020). Purification, partial structural characterization and health benefits of exopolysaccharides from potential probiotic Pediococcus acidilactici NCDC 252. Process Biochemistry, 99, 79-86. https://doi.org/10.1016/j.procbio.2020.08.028
29. Kwon, M., Lee, J., Park, S., Kwon, O. H., Seo, J., & Roh, S. (2020). Exopolysaccharide isolated from Lactobacillus plantarum l-14 has anti-inflammatory effects via the tolllike receptor 4 pathway in lps-induced raw 264.7 cells. International Journal of Molecular Sciences, 21(23), 1–18. https://doi.org/10.3390/ijms21239283
30. Laws, A., Gu, Y., & Marshall, V. (2001). Biosynthesis, characterisation, and design of bacterial exopolysaccharides from lactic acid bacteria. Biotechnology Advances, 19(8), 597-625. https://doi.org/10.1016/s0734-9750(01)00084-2
31. Li, J. Y., Jin, M. M., Meng, J., Gao, S. M., & Lu, R. R. (2013). Exopolysaccharide from Lactobacillus plantarum LP6: Antioxidation and the effect on oxidative stress. Carbohydrate Polymers, 98, 1147–1152. https://doi.org/10.1016/j.carbpol.2013.07.027
32. Li, S., & Shah, N. P. (2016). Characterization, anti-Inflammatory and antiproliferative activities of natural and sulfonated exopolysaccharides from Streptococcus thermophilus ASCC 1275. Journal of Food Science, 81(5), M1167–M1176. https://doi.org/10.1111/1750-3841.13276
33. Li, W., Xia, X., Tang, W., Ji, J., Rui, X., Chen, X., Jiang, M., Zhou, J., Zhang, Q., & Dong, M. (2015). Structural characterization and anticancer activity of cell-bound exopolysaccharide from Lactobacillus helveticus MB2-1. Journal of Agricultural and Food Chemistry, 63(13), 3454-3463. https://doi.org/10.1021/acs.jafc.5b01086
34. Liu, C. T., Chu, F. J., Chou, C. C., & Yu, R. C. (2011). Antiproliferative and anticytotoxic effects of cell fractions and exopolysaccharides from Lactobacillus casei 01. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 721(2), 157–162. https://doi.org/10.1016/j.mrgentox.2011.01.005
35. London, L. E. E., Kumar, A. H. S., Wall, R., Casey, P. G., O'Sullivan, O., Shanahan, F., Hill, C., Cotter, P. D., Fitzgerald, G. F., Ross, P. R., Caplice, N. M., & Stanton, C. (2014). Exopolysaccharide-producing probiotic Lactobacilli reduce serum cholesterol and modify enteric microbiota in ApoE-deficient mice. The Journal of Nutrition, 144(12), 1956-1962. https://doi.org/10.3945/jn.114.191627
36. Maeda, H., Zhu X., Omura, K., Suzuki, S., & Kitamura, S. (2004). Effects of an exopolysaccharide (kefiran) on lipids, blood pressure, blood glucose and constipation. Biofactors, 22, 197–200. https://doi.org/10.1002/biof.5520220141
37. Marcial, G., Villena, J., Faller, G., Hensel, A., & de Valdéz, G. F. (2017). Exopolysaccharide producing Streptococcus thermophilus CRL1190 reduces the inflammatory response caused by Helicobacter pylori. Beneficial Microbes, 8(3), 451-461. https://doi.org/10.3920/BM2016.0186
38. Minghetti, L. (2004). Cyclooxygenase-2 (COX-2) in inflammatory and degenerative brain diseases. Journal of Neuropathology and Experimental Neurology, 63(9), 901–910. https://doi.org/10.1093/jnen/63.9.901
39. Moradi, M., Mardani, K., & Tajik, H. (2019). Characterization and application of postbiotics of Lactobacillus spp. on Listeria monocytogenes in vitro and in food models. LWT-Food Science and Technology, 111, 457-464. https://doi.org/10.1016/j.lwt.2019.05.072
40. Noroozi, E., Tebianian, M., Taghizadeh, M., Dadar, M., & Mojgani, N. (2021). Anticarcinogenic potential of probiotic, postbiotic metabolites and paraprobiotics on human cancer cells. In N. Mojgani & M. Dadar (Eds.), Probiotic Bacteria and Postbiotic Metabolites: Role in Animal and Human Health (pp. 166). Springer.
41. Opal, S. M., & DePalo, V. A. (2000). Anti-inflammatory cytokines. Chest, 117(4), 1162–1172. https://doi.org/10.1378/chest.117.4.1162
42. Öner, E. T., Hernández, L., & Combie, J. (2016). Review of Levan polysaccharide: From a century of past experiences to future prospects. Biotechnology Advances, 34(5), 827–844. https://doi.org/10.1016/j.biotechadv.2016.05.002
43. Perricone, M., Bevilacqua, A., Corbo, M. R., & Sinigaglia, M. (2014). Technological characterization and probiotic traits of yeasts isolated from Altamura sourdough to select promising microorganisms as functional starter cultures for cereal-based products. Food Microbiology, 38, 26-35. https://doi.org/10.1016/j.fm.2013.08.006
44. Prado, M. R. M., Boller, C., Zibetti, R. G. M., de Souza, D., Pedroso, L. L., & Soccol, C. R. (2016). Anti-inflammatory and angiogenic activity of polysaccharide extract obtained from Tibetan kefir. Microvascular Research, 108, 29–33. https://doi.org/10.1016/j.mvr.2016.07.004
45. Rana, S., & Upadhyay, L. S. B. (2020). Microbial exopolysaccharides: Synthesis pathways, types and their commercial applications. International Journal of Biological Macromolecules, 15(157), 577-583. https://doi.org/10.1016/j.ijbiomac.2020.04.084
46. Rajoka, M. S. R., Wu, Y., Mehwish, H. M., Bansal, M., & Zhao, L. (2020). Lactobacillus exopolysaccharides: New perspectives on engineering strategies, physiochemical functions, and immunomodulatory effects on host health. Trends in Food Science & Technology, 103, 36-48. https://doi.org/10.1016/j.tifs.2020.06.003
47. Ren, W., Xia, Y., Wang, G., Zhang, H., Zhu, S., & Ai, L. (2016). Bioactive exopolysaccharides from a S. thermophilus strain: Screening, purification and characterization. International Journal of Biological Macromolecules, 86, 402-407. https://doi.org/10.1016/j.ijbiomac.2016.01.085
48. Rodríguez, C., Medici, M., Rodríguez, A. V., Mozzi, F., & de Valdez, G. F. (2009). Prevention of chronic gastritis by fermented milks made with exopolysaccharide-producing Streptococcus thermophilus strains. Journal of Dairy Science, 92(6), 2423-2434. https://doi.org/10.3168/jds.2008-1724
49. Ruas-Madiedo, P., & De Los Reyes-Gavilán, C. G. (2005). Invited review: Methods for the screening, isolation, and characterization of exopolysaccharides produced by lactic acid bacteria. Journal of Dairy Science, 88(3), 843-856. https://doi.org/10.3168/jds.S0022-0302(05)72750-8
50. Ruas-Madiedo, P. (2014). Food oligosaccharides: Production, analysis and bioactivity; Biosynthesis and bioactivity of exopolysaccharides produced by probiotic bacteria. In F.L. Moreno & M.L. Sanz (Eds.), Food oligosaccharides production, analysis and bioactivity (pp. 118-133). John Wiley & Sons, West Sussex.
51. Ryan, P., Ross, R., Fitzgerald, G., Caplice, N., & Stanton, C. (2015). Sugar-coated:exopolysaccharide producing lactic acid bacteria for food and human health applications. Food &Function, 6, 679–693. https://doi.org/10.1039/C4fo00529e
52. Saadat, Y. R., Khosroushahi, A. Y., & Gargari, B. P. A. (2019). A comprehensive review of anticancer, immunomodulatory and health beneficial effects of the lactic acid bacteria exopolysaccharides, Carbohydrate Polymers, 217, 79-89. https://doi.org/10.1016/j.carbpol.2019.04.025
53. Salazar, N., Gueimonde, M., Hernández-Barranco, A. M., Ruas-Madiedo, P., & de los ReyesGavilán, C. G. (2008). Exopolysaccharides produced by intestinal Bifidobacterium strains act as fermentable substrates for human intestinal bacteria. Applied and Environmental Microbiology, 74(15), 4737–4745. https://doi.org/ 10.1128/AEM.00325-08
54. Sanlibaba, P., & Çakmak, G. A. (2016). Exopolysaccharides production by lactic acid bacteria. Applied Microbiology, 2(2), 1-5. https://doi.org/10.4172/2471-9315.1000115
55. Schilling, C., Badri, A., Sieber, V., Koffas, M., & Schmid, J. (2020). Metabolic engineering for production of functional polysaccharides. Current Opinion in Biotechnology, 66, 44-51. https://doi.org/10.1016/j.copbio.2020.06.010
56. Tang, W., Dong, M., Wang, W., Han, S., Rui, X., Chen, X., Jiang, M., Zhang, Q., Junjun, W., & Li, W. (2017). Structural characterization and antioxidant property of released exopolysaccharides from Lactobacillus delbrueckii ssp. bulgaricus SRFM-1. Carbohydrate polymers, 173, 654-664. https://doi.org/10.1016/j.carbpol.2017.06.039
57. Taylan, O., Yilmaz, M. T., & Dertli, E. (2019). Partial characterization of a levan type exopolysaccharide (EPS) produced by Leuconostoc mesenteroides showing immunostimulatory and antioxidant activities. International Journal of Biological Macromolecules, 136, 436-444. https://doi.org/10.1016/j.ijbiomac.2019.06.078
58. Teame, T., Wang, A., Xie, M., Zhang, Z., Yang, Y., Ding, Q., Gao, C., Olsen, R. E., Ran, C., & Zhigang, Z. (2020). Paraprobiotics and postbiotics of probiotic Lactobacilli, their positive effects on the host and action mechanisms: A review. Frontiers in Nutrition, 7, 1-16. https://doi.org/10.3389/fnut.2020.570344
59. Thantsha, M. S., Mamvura, C. I., & Booyens, J. (2012). Probiotics–what they are, their benefits and challenges. In T. Brzozowski (Ed.). New Advances in the Basic and Clinical Gastroenterology (pp. 21-50). InTech: Croatia.
60. Uchida, M., Ishii, I., Inoue, C., Akisato, Y., Watanabe, K., Hosoyama, S., Toida, T., Ariyoshi, N., & Kitada, M. (2010). Kefiran reduces atherosclerosis in rabbits fed a high cholesterol diet. Journal of Atherosclerosis and Thrombosis, 17, 980–988. https://doi.org/10.5551/jat.4812
61. Venkatesha, S. H., Acharya, B., & Moudgil, K. D. (2017). Natural Products as Source of AntiInflammatory Drugs. In J.M. Cavaillon & M. Singer (Eds.), Inflammation - From Molecular and Cellular Mechanisms to the Clinic (pp. 1661-1690). Wiley.
62. 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. International Journal of Biological Macromolecules, 63, 133–139. https://doi.org/10.1016/j.ijbiomac.2013.10.036
63. Wang, J., Fang, X., Wu, T., Min, W., & Yang, Z. (2018). Exopolysaccharide producing Lactobacillus plantarum SKT109 as adjunct culture in Cheddar cheese production. LWT-Food Science and Technology, 97, 419-426. https://doi.org/10.1016/j.lwt.2018.07.011
64. Ye, G., Li, G., Wang, C., Ling, B., Yang, R., & Huang, S. (2019). Extraction and characterization of dextran from Leuconostoc pseudomesenteroides YB-2 isolated from mango juice. Carbohydrate polymers, 207, 218-223. https://doi.org/10.1016/j.carbpol.2018.11.092
65. Yu, Y. J., Chen, Z., Chen, P. T., & Ng, I. S. (2018). Production, characterization and antibacterial activity of exopolysaccharide from a newly isolated Weissella cibaria under sucrose effect. Journal of Bioscience and Bioengineering, 126(6), 769-777. https://doi.org/10.1016/j.biosc.2018.05.028
66. Zannini, E., Waters, D. M., Coffey, A., & Arendt, E. K. (2016). Production, properties, and industrial food application of lactic acid bacteria-derived exopolysaccharides. Applied Microbiology and Biotechnology,100(3),1121-1135.https://doi.org/10.007/s00253-015-7172-2
67. Zhang, G., Zhang, W., Sun, L., Sadiq, F. A., Yang, Y., Gao, J., & Sang, Y. (2019). Preparation screening, production optimization and characterization of exopolysaccharides produced by Lactobacillus sanfranciscensis Ls-1001 isolated from Chinese traditional sourdough. International Journal of Biological macromolecules, 139, 1295-1303. https://doi.org/10.1016/j.ijbiomac.2019.08.077
68. Zhang, Z., Liu, Z., Tao, X., & Wei, H. (2016). Characterization and sulfated modification of an exopolysaccharide from Lactobacillus plantarum ZDY2013 and its biological activities. Carbohydrate polymers, 153, 25-33. https://doi.org/10.1016/j.carbpol.2016.07.084
69. Zhou, Y., Cui, Y., & Qu, X. (2019). Exopolysaccharides of lactic acid bacteria: Structure, bioactivity and associations: A review. Carbohydrate Polymers, 207, 317-332. https://doi.org/10.1016/j.carbpol.2018.11.093