Abstract
Exopolysaccharide (EPS)-producing Bifidobacterium bifidum EPS DA-LAIM was isolated from healthy human feces, the structure of purified EPS from the strain was analyzed, and its prebiotic activity was evaluated. The EPS from B. bifidum EPS DA-LAIM is a glucomannan-type heteropolysaccharide with a molecular weight of 407–1007 kDa, and its structure comprises 2-mannosyl, 6-mannosyl, and 2,6-mannosyl residues. The purified EPS promoted the growth of representative lactic acid bacteria and bifidobacterial strains. Bifidobacterium bifidum EPS DA-LAIM increased nitric oxide production in RAW 264.7 macrophage cells, indicating its immunostimulatory activity. Bifidobacterium bifidum EPS DA-LAIM also exhibited high gastrointestinal tract tolerance, gut adhesion ability, and antioxidant activity. These results suggest that EPS from B. bifidum EPS DA-LAIM is a potentially useful prebiotic material, and B. bifidum EPS DA-LAIM could be applied as a probiotic candidate.
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References
Altmann F, Kosma P, O’Callaghan A, Leahy S, Bottacini F, Molloy E, Plattner S, Schiavi E, Gleinser M, Groeger D. Genome analysis and characterisation of the exopolysaccharide produced by Bifidobacterium longum subsp. longum 35624™. PloS one. 11: e0162983 (2016)
Alves EF, Bose SK, Francis RC, Colodette JL, Iakovlev M, Van Heiningen A. Carbohydrate composition of eucalyptus, bagasse and bamboo by a combination of methods. Carbohydrate Polymers. 82: 1097-1101 (2010)
Amiri S, Mokarram RR, Khiabani MS, Bari MR, Khaledabad MA. Exopolysaccharides production by Lactobacillus acidophilus LA5 and Bifidobacterium animalis subsp. lactis BB12: optimization of fermentation variables and characterization of structure and bioactivities. International Journal of Biological Macromolecules. 123: 752-765 (2019)
Ayaz F. Ruthenium based photosensitizer exerts immunostimulatory and possible adjuvant role on the mammalian macrophages in vitro. Cumhuriyet Science Journal CSJ. 39: 991-998 (2018)
Bogdan C. Nitric oxide and the immune response. Nature Immunology. 2: 907-916 (2001)
Brink M, Todorov S, Martin J, Senekal M, Dicks L. The effect of prebiotics on production of antimicrobial compounds, resistance to growth at low pH and in the presence of bile, and adhesion of probiotic cells to intestinal mucus. Journal of Applied Microbiology. 100: 813-820 (2006)
Castro-Bravo N, Wells JM, Margolles A, Ruas-Madiedo P. Interactions of surface exopolysaccharides from Bifidobacterium and Lactobacillus within the intestinal environment. Frontiers in Microbiology. 9: 2426 (2018)
Coakley M, Banni S, Johnson MC, Mills S, Devery R, Fitzgerald G, Paul Ross R, Stanton C. Inhibitory effect of conjugated α-linolenic acid from bifidobacteria of intestinal origin on SW480 cancer cells. Lipids. 44: 249-256 (2009)
Daba GM, Elnahas MO, Elkhateeb WA. Contributions of exopolysaccharides from lactic acid bacteria as biotechnological tools in food, pharmaceutical, and medical applications. International Journal of Biological Macromolecules. 173: 79-89 (2021)
EFSA Panel on Additives and Products of Substances used in Animal Feed (FEEDAP). Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA Journal. 10: 2740 (2012)
EFSA Panel on Additives Products or Substances used in Animal Feed (FEEDAP), Rychen G, Aquilina G, Azimonti G, Bampidis V, Bastos MDL, Bories G, Chesson A, Cocconcelli PS, Flachowsky G, Gropp J, Kolar B, Kouba M, López-Alonso M, Puente SL, Mantovani A, Mayo B, Ramos F, Saarela M, Villa RE, Wallace RJ, Wester P, Glandorf B, Herman L, Kärenlampi S, Aguilera J, Anguita M, Brozzi R, Galobart J. Guidance on the characterisation of microorganisms used as feed additives or as production organisms. EFSA Journal. 16: e05206 (2018)
Fanning S, Hall LJ, Cronin M, Zomer A, MacSharry J, Goulding D, O'Connell Motherway M, Shanahan F, Nally K, Dougan G. Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proceedings of the National Academy of Sciences. 109: 2108-2113 (2012)
Flemming H, Wingender J. The biofilm matrix. Nature Review Microbiology. 8: 623-633 (2010)
Garrigues C, Johansen E, Pedersen MB. Complete genome sequence of Bifidobacterium animalis subsp. lactis BB-12, a widely consumed probiotic strain. Journal of Bacteriology. 192: 2467-2468 (2010)
Gibson GR, Hutkins RW, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, Verbeke K, Reid G. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nature Reviews Gastroenterology & Hepatology. 14: 491-502 (2017)
González-Rodríguez I, Sánchez B, Ruiz L, Turroni F, Ventura M, Ruas-Madiedo P, Gueimonde M, Margolles A. Role of extracellular transaldolase from Bifidobacterium bifidum in mucin adhesion and aggregation. Applied and Environmental Microbiology. 78: 3992-3998 (2012)
He K, Bauer CE. Chemosensory signaling systems that control bacterial survival. Trends in Microbiology. 22: 389-398 (2014)
Hemmerich S, Bertozzi CR, Leffler H, Rosen SD. Identification of the sulfated monosaccharides of GlyCAM-1, an endothelial-derived ligand for L-selectin. Biochemistry. 33: 4820-4829 (1994)
Hidalgo-Cantabrana C, Sánchez B, Álvarez-Martín P, López P, Martínez-Álvarez N, Delley M, Martí M, Varela E, Suárez A, Antolín M. A single mutation in the gene responsible for the mucoid phenotype of Bifidobacterium animalis subsp. lactis confers surface and functional characteristics. Applied and Environmental Microbiology. 81: 7960-7968 (2015)
Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews Gastroenterology & Hepatology. 11: 506-514 (2014)
Korcz E, Kerényi Z, Varga L. Dietary fibers, prebiotics, and exopolysaccharides produced by lactic acid bacteria: potential health benefits with special regard to cholesterol-lowering effects. Food & Function. 9: 3057-3068 (2018)
Kwon A, ParkYS. Immunostimulatory activity of synbiotics using Lactococcus lactis SG-030 and glucooligosaccharides from Weissella cibaria YRK005. Microorganisms. 9: 2437 (2021)
Lin M-Y, Chang F-J. Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Digestive Diseases and Sciences. 45: 1617-1622 (2000)
Nachtigall C, Surber G, Bulla J, Rohm H, Jaros D. Pilot scale isolation of exopolysaccharides from Streptococcus thermophilus DGCC7710: Impact of methodical details on macromolecular properties and technofunctionality. Engineering in Life Sciences. 21: 220-232 (2021)
Nakajima H, Suzuki Y, Hirota T. Cholesterol loweing activity of ropy fermented milk. Journal of Food Science. 57: 1327-1329 (1992)
Panagiotopoulos C, Sempere R, Lafont R, Kerherve P. Sub-ambient temperature effects on the separation of monosaccharides by high-performance anion-exchange chromatography with pulse amperometric detection: Application to marine chemistry. Journal of Chromatography A. 920: 13-22 (2001)
Ruas-Madiedo P, Sánchez B, Hidalgo-Cantabrana C, Margolles A, Laws A. Exopolysaccharides from lactic acid bacteria and bifidobacteria. pp. 125-151. In: Handbook of Animal Based Fermented Food and Beverage Technology. Hui YH, Evranuz EO (eds). CRC Press, Inc., Boca Raton, FL, USA (2012)
Ryan P, Ross R, Fitzgerald G, Caplice N, Stanton C. Sugar-coated: exopolysaccharide producing lactic acid bacteria for food and human health applications. Food & Function. 6: 679-693 (2015)
Saadat YR, Khosroushahi AY, Gargari BP. A comprehensive review of anticancer, immunomodulatory and health beneficial effects of the lactic acid bacteria exopolysaccharides. Carbohydrate Polymers. 217: 79-89 (2019)
Serafini F, Strati F, Ruas-Madiedo P, Turroni F, Foroni E, Duranti S, Milano F, Perotti A, Viappiani A, Guglielmetti S. Evaluation of adhesion properties and antibacterial activities of the infant gut commensal Bifidobacterium bifidum PRL2010. Anaerobe. 21: 9-17 (2013)
Sharma A, Kaur J, Lee S, Park YS. Tracking of deliberately inoculated Leuconostoc mesenteroides and Lactobacillus brevis in kimchi. Food Science and Biotechnology. 29: 817–824 (2020)
Takahashi N, Xiao J-Z, Miyaji K, Yaeshiima T, Hiramatsu A, Iwatsuki K, Kokubo S, Hosono A. Selection of acid tolerant bifidobacteria and evidence for a low-pH-inducible acid tolerance response in Bifidobacterium longum. Journal of Dairy Research. 71: 340-345 (2004)
Turchi B, Mancini S, Fratini F, Pedonese F, Nuvoloni R, Bertelloni F, Ebani VV, Cerri D. Preliminary evaluation of probiotic potential of Lactobacillus plantarum strains isolated from Italian food products. World Journal of Microbiology and Biotechnology. 29: 1913-1922 (2013)
Vossenkämper A, Marchès O, Fairclough P, Warnes G, Stagg A, Lindsay J, Evans P, Luong L, Croft N, Naik S, Frankel G,MacDonald T. Inhibition of NF-κB signaling in human dendritic cells by the enteropathogenic Escherichia coli effector protein NleE. Journal of Immunology. 185: 4118-4127 (2010)
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Kang, M.J., Jeong, H., Kim, S. et al. Structural analysis and prebiotic activity of exopolysaccharide produced by probiotic strain Bifidobacterium bifidum EPS DA-LAIM. Food Sci Biotechnol 32, 517–529 (2023). https://doi.org/10.1007/s10068-022-01213-w
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DOI: https://doi.org/10.1007/s10068-022-01213-w