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Improved functionality of fermented milk is mediated by the synbiotic interaction between Cudrania tricuspidata leaf extract and Lactobacillus gasseri strains

  • Applied microbial and cell physiology
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Abstract

This study was designed to investigate the cooperative effect of selected Lactobacillus gasseri strains and Cudrania tricuspidata (CT) leaf extract in enhancing the health-promoting activities of fermented milk. Addition of CT increased total bacterial counts and proteolysis during fermentation of milk with L. gasseri strains. Antioxidant capacities were determined by measuring the ABTS, DPPH, and peroxyl radical scavenging activities and ferric reducing power. The antioxidant capacity of CT-supplemented milk was greater than that of milk without supplementation; moreover, the antioxidant activity of CT-supplemented milk was synergistically improved by fermentation with L. gasseri strains. In particular, CT-supplemented milk fermented by L. gasseri 505 showed the highest antioxidant activity. The phenolic compounds in CT, such as neo-chlorogenic, chlorogenic, and caffeic acid, were metabolized during fermentation with L. gasseri strains, and 3,4-dihydroxy-hydrocinnamic acid was produced as a fermentation metabolite. Moreover, the liberation of bioactive peptides of fermented milk was increased by the proteolytic activity of L. gasseri strains. In particular, six peptides, which were mainly derived from β-casein, were newly identified in this study. These findings suggest that L. gasseri strains metabolize the phenolic acids in the CT and the bioactive peptides released through this interaction improve the antioxidant activity of the fermented milk.

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References

  • Arakawa K, Kawai Y, Fujitani K, Nishimura J, Kitazawa H, Komine K, Kai K, Saito T (2008) Bacteriocin production of probiotic Lactobacillus gasseri LA39 isolated from human feces in milk-based media. Anim Sci J 79(5):634–640

    Article  CAS  Google Scholar 

  • Arakawa K, Kawai Y, Ito Y, Nakamura K, Chujo T, Nishimura J, Kitazawa H, Saito T (2010) HPLC purification and re-evaluation of chemical identity of two circular bacteriocins, gassericin A and reutericin 6. Lett Appl Microbiol 50(4):406–411

    Article  CAS  PubMed  Google Scholar 

  • Argyri AA, Zoumpopoulou G, Karatzas K-AG, Tsakalidou E, Nychas G-JE, Panagou EZ, Tassou CC (2013) Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol 33(2):282–291

    Article  CAS  PubMed  Google Scholar 

  • Axelsson L (2004) Lactic acid bacteria: classification and physiology. Food Science and Technology-New York-Marcel Dekker 139:1–66

  • Bajpai VK, Sharma A, Baek K-H (2013) Antibacterial mode of action of Cudrania tricuspidata fruit essential oil, affecting membrane permeability and surface characteristics of food-borne pathogens. Food Control 32(2):582–590

    Article  CAS  Google Scholar 

  • Bindels LB, Delzenne NM, Cani PD, Walter J (2015) Towards a more comprehensive concept for prebiotics. Nat Rev Gastro Hepat 12(5):303–310

    Article  CAS  Google Scholar 

  • Chang OK, Roux É, Awussi AA, Miclo L, Jardin J, Jameh N, Dary A, Humbert G, Perrin C (2014) Use of a free form of the Streptococcus thermophilus cell envelope protease PrtS as a tool to produce bioactive peptides. Int Dairy J 38(2):104–115

    Article  CAS  Google Scholar 

  • Choi S-R, You D-H, Kim J-Y, Park C-B, Kim D-H, Ryu J, Choi D-G, Park H-M (2009) Antimicrobial activity of methanol extracts from Cudrania tricuspidata bureau according to the parts harvested and time. Korean J Med Crop Sci 17(5):335–340

    Google Scholar 

  • Christensen JE, Dudley EG, Pederson JA, Steele JL (1999) Peptidases and amino acid catabolism in lactic acid bacteria. Antonie Van Leeuwenhoek 76(1–4):217–246

  • Couteau D, McCartney A, Gibson G, Williamson G, Faulds C (2001) Isolation and characterization of human colonic bacteria able to hydrolyse chlorogenic acid. J Appl Microbiol 90(6):873–881

    Article  CAS  PubMed  Google Scholar 

  • Ebner J, Arslan AA, Fedorova M, Hoffmann R, Küçükçetin A, Pischetsrieder M (2015) Peptide profiling of bovine kefir reveals 236 unique peptides released from caseins during its production by starter culture or kefir grains. J Proteome 117:41–57

    Article  CAS  Google Scholar 

  • Fuglsang A, Nilsson D, Nyborg NC (2003) Characterization of new milk-derived inhibitors of angiotensin converting enzyme in vitro and in vivo. J Enzym Inhib Med Ch 18(5):407–412

    Article  CAS  Google Scholar 

  • Gobbetti M, Cagno RD, De Angelis M (2010) Functional microorganisms for functional food quality. Crit Rev Food Sci 50(8):716–727

    Article  CAS  Google Scholar 

  • Gobbetti M, Ferranti P, Smacchi E, Goffredi F, Addeo F (2000) Production of angiotensin-I-converting-enzyme-inhibitory peptides in fermented milks started by Lactobacillus delbrueckii subsp. bulgaricus SS1 and Lactococcus lactis subsp. cremoris FT4. App Environ Microb 66(9):3898–3904

    Article  CAS  Google Scholar 

  • Hassaninasab A, Hashimoto Y, Tomita-Yokotani K, Kobayashi M (2011) Discovery of the curcumin metabolic pathway involving a unique enzyme in an intestinal microorganism. P Natl Acad Sci USA 108(16):6615–6620

    Article  CAS  Google Scholar 

  • Hayes M, Stanton C, Slattery H, O'Sullivan O, Hill C, Fitzgerald G, Ross R (2007) Casein fermentate of Lactobacillus animalis DPC6134 contains a range of novel propeptide angiotensin-converting enzyme inhibitors. App Environ Microb 73(14):4658–4667

    Article  CAS  Google Scholar 

  • Hernández-Ledesma B, Amigo L, Ramos M, Recio I (2004) Angiotensin converting enzyme inhibitory activity in commercial fermented products. Formation of peptides under simulated gastrointestinal digestion. J Agr Food Chem 52(6):1504–1510

    Article  Google Scholar 

  • Huang Y, Wang X, Wang J, Wu F, Sui Y, Yang L, Wang Z (2013) Lactobacillus plantarum strains as potential probiotic cultures with cholesterol-lowering activity. J Dairy Sci 96(5):2746–2753

    Article  CAS  PubMed  Google Scholar 

  • Hui YH, Meunier-Goddik L, Josephsen J, Nip W-K, Stanfield PS (2004) Handbook of food and beverage fermentation technology, vol 134. CRC, New York

    Book  Google Scholar 

  • Jae-Young C (2000) Effects of water-soluble extract from leaves of Morus alba and Cudrania tricuspidata on the lipid peroxidation in tissues of rats. J Korean Soc Food Sci Nutr 29(3):531–536

    Google Scholar 

  • Jaya S, Das H (2004) Effect of maltodextrin, glycerol monostearate and tricalcium phosphate on vacuum dried mango powder properties. J Food Eng 63(2):125–134

    Article  Google Scholar 

  • Jeong C-H, Choi GN, Kim JH, Kwak JH, Heo HJ, Shim K-H, Cho B-R, Bae Y-I, Choi J-S (2009) In vitro antioxidative activities and phenolic composition of hot water extract from different parts of Cudrania tricuspidata. J Food Sci Nutr 14(4):283–289

    Article  CAS  Google Scholar 

  • Johansson A, Lugand D, Rolet-Répécaud O, Mollé D, Delage M-M, Peltre G, Marchesseau S, Léonil J, Dupont D (2009) Epitope characterization of a supramolecular protein assembly with a collection of monoclonal antibodies: the case of casein micelle. Mol Immunol 46(6):1058–1066

    Article  CAS  PubMed  Google Scholar 

  • Kadooka Y, Sato M, Imaizumi K, Ogawa A, Ikuyama K, Akai Y, Okano M, Kagoshima M, Tsuchida T (2010) Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur J Clin Nutr 64(6):636–643

    Article  CAS  PubMed  Google Scholar 

  • Kawai Y, Saitoh B, Takahashi O, Kitazawa H, Saito T, Nakajima H, Itoh T (2000) Primary amino acid and DNA sequences of gassericin T, a lactacin F-family bacteriocin produced by Lactobacillus gasseri SBT2055. Biosci Biotechnol Biochem 64(10):2201–2208

    Article  CAS  PubMed  Google Scholar 

  • Kilara A, Panyam D (2003) Peptides from milk proteins and their properties. Crit Rev Food Sci 43(6):607–633

    Article  CAS  Google Scholar 

  • Kirilov N, Dimov S, Dalgalarrondo M, Ignatova T, Kambarev S, Stoyanovski S, Danova S, Iliev I, Haertlé T, Chobert J-M (2011) Characterization of enterococci isolated from homemade Bulgarian cheeses and katuk. Eur Food Res Technol 233(6):1029–1040

    Article  CAS  Google Scholar 

  • Lahov E, Regelson W (1996) Antibacterial and immunostimulating casein-derived substances from milk: casecidin, isracidin peptides. Food Chem Toxicol 34(1):131–145

    Article  CAS  PubMed  Google Scholar 

  • Lignitto L, Cavatorta V, Balzan S, Gabai G, Galaverna G, Novelli E, Sforza S, Segato S (2010) Angiotensin-converting enzyme inhibitory activity of water-soluble extracts of Asiago d’allevo cheese. Int Dairy J 20(1):11–17

    Article  CAS  Google Scholar 

  • Møller KK, Rattray FP, Ardö Y (2013) Application of selected lactic acid bacteria and coagulant for improving the quality of low-salt Cheddar cheese: chemical, microbiological and rheological evaluation. Int Dairy J 33(2):163–174

    Article  Google Scholar 

  • Maksimovic Z, Malencic D, Kovacevic N (2005) Polyphenol contents and antioxidant activity of Maydis stigma extracts. Bioresource Technol 96(8):873–877

    Article  CAS  Google Scholar 

  • Manning TS, Gibson GR (2004) Prebiotics. Best Pract Res Clin Gastroenterol 18(2):287–298

    Article  PubMed  Google Scholar 

  • Matar C, Goulet J (1996) β-casomorphin 4 from milk fermented by a mutant of Lactobacillus helveticus. Int Dairy J 6(4):383–397

    Article  CAS  Google Scholar 

  • Meisel H, FitzGerald R (2003) Biofunctional peptides from milk proteins: mineral binding and cytomodulatory effects. Curr Pharm Design 9(16):1289–1296

    Article  CAS  Google Scholar 

  • Miguel M, Recio I, Ramos M, Delgado M, Aleixandre M (2006) Antihypertensive effect of peptides obtained from Enterococcus faecalis-fermented milk in rats. J Dairy Sci 89(9):3352–3359

    Article  CAS  PubMed  Google Scholar 

  • Nakamura Y, Yamamoto N, Sakai K, Takano T (1995) Antihypertensive effect of sour milk and peptides isolated from it that are inhibitors to angiotensin I-converting enzyme. J Dairy Sci 78(6):1253–1257

    Article  CAS  PubMed  Google Scholar 

  • Nielsen PM, Petersen D, Dambmann C (2001) Improved method for determining food protein degree of hydrolysis. J Food Sci 66(5):642–646

    Article  CAS  Google Scholar 

  • Oh NS, Lee HA, Lee JY, Joung JY, Lee KB, Kim Y, Lee KW, Kim SH (2013) The dual effects of Maillard reaction and enzymatic hydrolysis on the antioxidant activity of milk proteins. J Dairy Sci 96(8):4899–4911. doi:10.3168/jds.2013-6613

    Article  CAS  PubMed  Google Scholar 

  • Osuntoki A, Korie I (2010) Antioxidant activity of whey from milk fermented with Lactobacillus species isolated from Nigerian fermented foods. Food Technol Biotech 48(4):505–511

    CAS  Google Scholar 

  • Park KH, Park Y-D, Han J-M, Im K-R, Lee BW, Jeong IY, Jeong T-S, Lee WS (2006) Anti-atherosclerotic and anti-inflammatory activities of catecholic xanthones and flavonoids isolated from Cudrania tricuspidata. Bioorg Med Chem Lett 16(21):5580–5583

    Article  CAS  PubMed  Google Scholar 

  • Queipo-Ortuño MI, Boto-Ordóñez M, Murri M, Gomez-Zumaquero JM, Clemente-Postigo M, Estruch R, Diaz FC, Andrés-Lacueva C, Tinahones FJ (2012) Influence of red wine polyphenols and ethanol on the gut microbiota ecology and biochemical biomarkers. Am J Clin Nutr 95(6):1323–1334

    Article  PubMed  Google Scholar 

  • Quirós A, Ramos M, Muguerza B, Delgado MA, Miguel M, Aleixandre A, Recio I (2007) Identification of novel antihypertensive peptides in milk fermented with Enterococcus faecalis. Int Dairy J 17(1):33–41

    Article  Google Scholar 

  • Recio I, Visser S (1999) Identification of two distinct antibacterial domains within the sequence of bovine α s2-casein. Biochim Biophys Acta-General Subjects 1428(2):314–326

    Article  CAS  Google Scholar 

  • Regazzo D, Mollé D, Gabai G, Tomé D, Dupont D, Leonil J, Boutrou R (2010) The (193–209) 17-residues peptide of bovine β-casein is transported through Caco-2 monolayer. Mol Nutr Food Res 54(10):1428–1435

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Amaya DB (2010) Quantitative analysis, in vitro assessment of bioavailability and antioxidant activity of food carotenoids—a review. J Food Compos Anal 23(7):726–740

    Article  CAS  Google Scholar 

  • Roy MK, Koide M, Rao TP, Okubo T, Ogasawara Y, Juneja LR (2010) ORAC and DPPH assay comparison to assess antioxidant capacity of tea infusions: relationship between total polyphenol and individual catechin content. Int J Food Sci Nutr 61(2):109–124

    Article  CAS  PubMed  Google Scholar 

  • Ścibisz I, Ziarno M, Mitek M, Zaręba D (2012) Effect of probiotic cultures on the stability of anthocyanins in blueberry yoghurts. LWT-Food Sci Technol 49(2):208–212

    Article  Google Scholar 

  • Selle K, Klaenhammer TR (2013) Genomic and phenotypic evidence for probiotic influences of Lactobacillus gasseri on human health. FEMS Microbiol Rev 37(6):915–935

    Article  CAS  PubMed  Google Scholar 

  • Seo EJ, Curtis-Long MJ, Lee BW, Kim HY, Ryu YB, Jeong T-S, Lee WS, Park KH (2007) Xanthones from Cudrania tricuspidata displaying potent α-glucosidase inhibition. Bioorg Med Chem Lett 17(23):6421–6424

    Article  CAS  PubMed  Google Scholar 

  • Thaipong K, Boonprakob U, Crosby K, Cisneros-Zevallos L, Byrne DH (2006) Comparison of ABTS, DPPH, FRAP, and ORAC assays for estimating antioxidant activity from guava fruit extracts. J Food Compos Anal 19(6):669–675

    Article  CAS  Google Scholar 

  • Tzounis X, Rodriguez-Mateos A, Vulevic J, Gibson GR, Kwik-Uribe C, Spencer JP (2011) Prebiotic evaluation of cocoa-derived flavanols in healthy humans by using a randomized, controlled, double-blind, crossover intervention study. Am J Clin Nutr 93(1):62–72

    Article  CAS  PubMed  Google Scholar 

  • Van Duynhoven J, Vaughan EE, Jacobs DM, Kemperman RA, Van Velzen EJ, Gross G, Roger LC, Possemiers S, Smilde AK, Doré J (2011) Metabolic fate of polyphenols in the human superorganism. P Natl Acad Sci USA 108(Supplement 1):4531–4538

  • Virtanen T, Pihlanto A, Akkanen S, Korhonen H (2007) Development of antioxidant activity in milk whey during fermentation with lactic acid bacteria. J Appl Microbiol 102(1):106–115

    Article  CAS  PubMed  Google Scholar 

  • Vodnar DC, Socaciu C (2012) Green tea increases the survival yield of Bifidobacteria in simulated gastrointestinal environment and during refrigerated conditions. Chem Cent J 6(1):61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto N, Akino A, Takano T (1994) Antihypertensive effect of the peptides derived from casein by an extracellular proteinase from Lactobacillus helveticus CP790. J Dairy Sci 77(4):917–922

    Article  CAS  PubMed  Google Scholar 

  • Zainoldin K, Baba A (2009) The effect of Hylocereus polyrhizus and Hylocereus undatus on physicochemical, proteolysis, and antioxidant activity in yogurt. World Acad Sci Eng Technol 60:361–366

    Google Scholar 

  • Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64(4):555–559

    Article  CAS  Google Scholar 

  • Zou Y-S, Hou A-J, Zhu G-F, Chen Y-F, Sun H-D, Zhao Q-S (2004) Cytotoxic isoprenylated xanthones from Cudrania tricuspidata. Bioorgan Med Chem 12(8):1947–1953

    Article  CAS  Google Scholar 

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Correspondence to Younghoon Kim.

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This study was funded by the High Value-Added Food Technology Development Program of the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry, and Fisheries (iPET) and the Ministry for Food, Agriculture, Forestry, and Fisheries of Republic of Korea (313036-03-2-SB010) and the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education (2014R1A1A2008481 to S.O.)

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The authors declare that they have no competing interests.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Nam Su Oh and Ji Young Lee contributed equally to this study.

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Oh, N.S., Lee, J.Y., Oh, S. et al. Improved functionality of fermented milk is mediated by the synbiotic interaction between Cudrania tricuspidata leaf extract and Lactobacillus gasseri strains. Appl Microbiol Biotechnol 100, 5919–5932 (2016). https://doi.org/10.1007/s00253-016-7414-y

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  • DOI: https://doi.org/10.1007/s00253-016-7414-y

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