Biotransformation of ferulic acid by Lactobacillus acidophilus K1 and selected Bifidobacterium strains

• Autorzy: Szwajgier D. , Jakubczyk A.

Warianty tytułu

PL

Biotransformacja kwasu ferulowego przez bakterie Lactobacillus acidophilus K1 oraz wybrane bakterie z rodzaju Bifidobacterium

• Języki publikacji: EN

Abstrakty

EN

Background. Lactic acid bacteria (LAB) were pointed out to produce ferulic acid es- terase. Except the release of phenolic acids front esterified forms, it was postulated that the biotransformations of these compounds can occur during the bacterial growth. In the presented work, the biotransformation of ferulic acid by Lactobacillus acidophilus KI and three Bifidibacterium strains (B. animalis Bi30, B. catenulatum KD 14 and B. longum KN 29) was studied. Material and methods. The microorganisms were grown in media containing methyl esters of phenolic acids as carbon sources. The feruloyl esterase activity as well as the contents of phenolic acids in supematants were estimated using HPLC-DAD. Results. The enzyme activity was evaluated using methyl ferulate exclusively, but p- -coumaric acid and another chromatographic peak (probably caffeic acid, but its identity was not positively confirmed by the DAD analysis) were present in reaction mixtures containing the supematants of Lactobacillus acidophilus KI cultivars with methyl p-coumarate or methyl syringate. Both peaks of p-coumaric acid and another phenolic compound were also present in the Solutions containing the supematants of B. catenulatum and B. longum grown in the presence of methyl vanillate and the supematants of B. animalis Bi30 grown using methyl p-coumarate, methyl syringate or methyl vanillate. Conclusions. The results suggest a distinct ability of the studied LAB strains to transform free ferulic acid yielding p-coumaric acid and probably caffeic acid although no mechanism involved in this transformation was proposed and closer characterised in the frames of this work.

PL

Wprowadzenie. Bakterie kwasu mlekowego były w przeszłości wskazywane jako producent esterazy kwasu ferulowego. Poza uwalnianiem kwasów fenolowych z form estrowych, wskazywano na możliwość biotransformacji kwasów fenolowych w czasie wzrostu bakterii. W pracy badano zdolność bakterii Lactobacillus acidophilus KI i trzech szczepów bakterii z rodzaju Bifidibacterium (B. animalis Bi30, B. catenulatum KD 14 i B. longum KN 29) do biotransformacji kwasu ferulowego. Materiał i metody. Drobnoustroje hodowano w pożywkach zawierających metylowe estry wybranych kwasów fenolowych jako jedyne źródło węgla. Aktywności esterazy kwasu ferulowego oraz zawartości kwasów fenolowych w supernatantach określano za pomocą techniki HPLC z detekcją DAD. Wyniki. Aktywność enzymatyczna była oznaczana wyłącznie z użyciem ferulanu metylu, ale w supernatantach pohodowlanych wszystkich bakterii stwierdzono obecność piku chromatograficznego kwasu p-kumarowego. Ponadto zarejestrowano dodatkowo jeden niezidentyfikowany pik (prawdopodobnie kwasu kawowego, jednak obecność tego związku nie została potwierdzona poprzez analizę widmową DAD) w próbach zawierających supernatant uzyskany po hodowlach bakterii Lactobacillus acidophilus KI z użyciem p-kumaranu metylu lub syringanu metylu. Obecność obu pików (kwasu p-kumarowego oraz niezidentyfikowany) stwierdzono również w obrazie chromatograficznym w czasie analizy supernatantów uzyskanych po hodowlach B. catenulatum i B. longum na wanilianie metylu i B. animalis Bi30 z użyciem p-kumaranu metylu, syringanu metylu lub waniliami metylu jako źródła węgla. Wnioski. Powyższe wyniki wskazują na zdolność badanych bakterii mlekowych do przekształcania kwasu ferulowego do kwasu p-kumarowego i prawdopodobnie kwasu kawowego, ale w pracy nie podjęto próby bliższego scharakteryzowania mechanizmów enzymatycznych biorących udział w omawianych transformacjach.

Słowa kluczowe

EN

biotransformation; ferulic acid; Lactobacillus acidophilus; Bifidobacterium; probiotic; antioxidant; lactic acid bacteria; K1 cultivar

• Wydawca: -
• Czasopismo: Acta Scientiarum Polonorum. Technologia Alimentaria
• Rocznik: 2010
• Tom: 09
• Numer: 1
• Opis fizyczny: p.45-59,fig.,ref.

Twórcy

autor

Szwajgier D.

• University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland

autor

Jakubczyk A.

Bibliografia

• Alberto M.R., Farias M.E., Manca De Nadra M.C., 2001. Effect of gallic acid and catechin on Lactobacillus hilgardii 5w growth and metabolism of organie compounds. J. Agric. Food Chem. 49, 4359-4363.
• Andreason M.F., Kroon P., Williamson G., Garcia-Conesa M.T., 2001. Esterase activity able to hydrolyze dietary antioxidant hydroxycinnamates is distributed along the intestine of mammals. J. Agric. Food Chem. 49, 5679-5684.
• Barthelmebs L., Divies C., Cavin J.F., 2001. Molecular characterization of the phenolic acid metabolism in the lactic acid bacteria Lactobacillus plantarum. Lait. 81, 161-171.
• Bhathena J., Kulamarva A., Martoni C., Urbańska A.M., Prakash S., 2008. Preparation and in vitro analysis of microencapsulated live Lactobacillus fermentum 11976 for augmentation of feruloyl esterase in the gastrointestinal tract. Biotechnol. Appl. Biochem. 50(1), 1-9.
• Biedrzycka E., Kielecka M., Wróblewska B., Jędrychowski L., Duńczyk Z., Heros C.M., 2003. Immunostimulative activity of probiotic Bifidobacterium strains determined In vivo using ELISA method. Pol. J. Food Nutr. Sci. 12(53), 20-23.
• Bielecka M., Biedrzycka E., Majkowska A., 2002. Selection of probiotics and prebiotics for synbiotics and confirmation of their in vivo effectiveness. Food Res. Int. 35, 125-131.
• Bloem A., Bertrand A., Lonvaud-Funel A., De Revel G., 2007. Vanillin production from simple phenols by wine-associated lactic acid bacteria. Lett. Appl. Microbiol. 44, 62-67.
• Boume L.C., Rice-Evans S.C., 1998. Bioavailability of ferulic acid. Biochem. Biophys. Res. Commun. 18, 253.
• Cavin J.F., Andioc V., Etievant P.X., Divies C., 1993. Ability of wine LAB to metabolize phenol carboxylic acids. Am. J. Enol. Vitic. 44, 76-80.
• Cavin J.-F., Barthelmebs L., Guzzo J., Van Beeumen J., Samyn B., Travers J.F., Divies C., 1997. Purification and characterization of an inducible p-coumaric acid decarboxylase from Lactobacillus plantarum. FEMS Microbiol. Lett. 147, 291-295.
• Chatonnet P., Dobourdieu D., Boidron J., 1995. The influence of Brettanomyces/Dekkera sp. yeast and LAB on the ethylphenol content of red wine. Am. J. Enol. Vitic. 46, 63-68.
• Chatonnet P., Viala C., Dubourdieu D., 1997. Influence of polyphenolic components of red wines on the microbial synthesis of volatile phenols. Am. J. Enol. Vitic. 48(4), 443-448.
• Choudhury R., Srai K., Debnam E., Rice-Evans C.A., 1999. Urinary excretion of hydroxycinnamates and flavonoids after oral and intravenous administration. Free Rad. Biol. Med. 27, 278- -286.
• Clavel T., Borrmann D., Braune A., Dore J., Blaut M., 2006. Occurence and activity of human intestinal bacteria involved in the conversion of dietary lignans. Anaerobe (Food Microbiol.) 12, 140-147.
• Clifford M.N., Copeland E.L., Bloxsidge J.P., Mitchell L.A., 2000. Hippuric acid as a major excretion product associated with black tea consumption. Xenobiotica 50, 317-326.
• Couteau D., Mccartney A.L., Gibson, G.R., Williamson G., Faulds CB., 2001. Isolation and characterization of human colonie bacteria able to hydrolase chlorogenic acid. J. Appl. Microbiol. 90, 873-881.
• Couto J.A., Campos F.M., Figueiredo A.R., Hogg T.A., 2006. Ability of lactic acid bacteria to produce volatile phenols. Am. J. Enol. Vitic. 57(2), 166-171.
• De Las Rivas B., Rodriguez H., Curiel J.A., Landete J.M., Munoz R., 2009. Molecular screening of wine lactic acid bacteria degrading hydroxycinnamic acids. J. Agric. Food Chem. 57, 490- -494.
• Deprez S., Brezillon C., Raport S., Philippe C., Mila I., Lapierre C., Scalbert A., 2000. Polymeric proanthocyanidins are catabolized by human colonie microflora into low-molecular-weight phenolic acids. J. Nutr. 130, 2733-2738.
• Donaghy J., Kelly P.F., Mckay A.M., 1998. Detection of ferulic acid esterase production by Bacillus spp and lactobacilli. Appl. Microbiol. Biotechnol. 50, 257-260.
• Dugelay I., Gunata Z., Sapis J.C., Baumes R., Bayonove C., 1993. Role of cinnamoyl esterase activities from enzyme preparations on the formation of volatile phenols during winemaking. J. Agric. Food Chem. 41, 2092-2096.
• Gerhäuser C., 2005. Beer constituents as potential cancer chemopreventive agents. Eur. J. Cancer. 41, 1941-1954.
• Ghiselli A., Natella F., Guidi A., Montanari L., Fantozzi P. Scaccini C., 2000. Beer increases plasma antioxidant capacity in humans. J. Nutr. Biochem. 11, 76-80.
• Gross M., Pfeiffer M., Martini M., Campbell D., Slavin J., Potter J., 1996. The quantitation of metabolites of quercetin flavonols in human urine. Cancer Epidemiol. Biomarkers Prev. 5, 711-720.
• Hemandez T., Estrella I., Perez-Gordo M., Alergia E.G., Tenorio C., Ruiz-Larrrea F., Moreno- Arribas, M.V., 2007. Contribution of malolactic fermentation by Oenococcus oeni and Lactobacillus plantarum to the changes in the anthocyanin polyphenolic composition of red wine. J. Agric. Food Chem. 55, 5260-5266.
• Hollman P.C., Katan M.B., 1998. Bioavailability and health effects of dietary flavonols in man. Arch. Toxicol. 20, 237-248.
• Itagaki S., Kurokawa T., Nakata C., Saito Y., Oikawa S., Kobayashi M., Hirano T., Iseki K., 2009. In vitro and in vivo antioxidant properties of ferulic acid. A comparative study with other natural oxidation inhibitors. Food Chem. 114(2), 466-471.
• Joshi G., Perluigi M., Sułtana R., Agrippino R., Calabrese V., Butterfield D.A., 2006. In vivo protection of synaptosomes by ferulic acid ethyl ester (FAEE) from oxidative stress mediated by 2,2-azobis(2-amidino-propane)dihydrochloride (AAPF1) or Fe2+/H202: Insight into mechanisms of neuroprotection and relevance to oxidative stress-related neurodegenerative disorders. Neurochem. Int. 48(4), 318-327.
• Kański J., Aksenova M., Stoyanova A., Butterfield D.A., 2002. Ferulic acid antioxidant protection against hydroxyl and peroxyl radical oxidation in synaptosomal and neuronal celi culture systems in vitro: structure-activity studies. J. Nutr. Biochem. 13, 273-281.
• Kim K.-H., Tsao R., Yang R., Cui S.W., 2006. Phenolic acid profiles and antioxidant activities of wheat bran extracts and the effect of hydrolysis conditions. Food Chem. 95, 466-473.
• Landete J.M., Curiel J.A., Rodriguez H., De La Rivas B., Munoz R., 2008. Study of the inhibitory activity of phenolic compounds found in olive products and their degradation by Lactobacillus plantarum strains. Food Chem. 107, 320-326.
• Maillard M.-N., Berset C., 1995. Evolution of antioxidant activity during kilning: role of insoluble bound phenolic acids of barley and malt. J. Agric. Food Chem. 43, 1789-1793.
• Maillard M.N., Soum M.FL, Boivin P., Berset C., 1996. Antioxidant activity of barley and malt: relationship with phenolic content. Lebensm.-Wiss. Technol. 29, 238-244.
• Mechichi T., Patel B.K.C., Sayadi S., 2005. Anaerobic degradation of methoxylated aromatic compounds by Clostridium methoxybenzovorans and a nitrate-reducing bacterium Thauera sp. Strain Cin3,4. Int. Biodeter. Biodegr. 56, 224-230.
• Micard V., Landazuri T., Surget A., Moukha S., Labat M., Rouau X., 2002. Demethylation of ferulic acid and feruloyl-arabinoxylan by microbial celi extracts. Lebensm.-Wiss. Technol. 35, 272-276.
• Nardini M., Cirillo E., Natella F., Scaccini C., 2002. Absorption of phenolic acids in humans after coffee consumption. J. Agric. Food Chem. 50, 5735-5741.
• Nardini M., D'aquino M., Tomassi G., Gentili V., Di Felice M., Scaccini C., 1995. Inhibition of human low-density lipoprotein oxidation by caffeic acid and other hydrocinnamic acid derivatives. Free Rad. Biol. Med. 19, 541-552.
• Nardini M., Natella F., Gentili V., Di Felice M., Scaccini C., 1997. Effect of caffeic acid dietary supplementation on the antioxidant defense system in rat: an in vivo study. Arch. Biochem. Biophys. 342(1), 157-160.
• Nardini M., Natella F., Scaccini C., Ghiselli A., 2006. Phenolic acids from beer are absorbed and extensively metabolized in humans. J. Nutr. Biochem. 17, 14-22.
• Nsereko V., Smiley B.K., Rutherford W.M., Spielbauer A., Forrester K.J., Hettinger G.H., Harman E.K., Harman B.R., 2008. Influence of inoculating forage with lactic acid bacterial strains that produce ferulate esterase on ensilage and ruminal degradation of fiber. Anim. Feed Sci. Tech. 145, 122-135.
• Olthof M.R., Hollman P.C., Bujisman M.N., Van Amelsvoort J.M., Katan M.B., 2003. Chlorogenic acid, quercetin-3-rutinoside and black tea phenols are extensively metabolised in humans. J.Nutr. 133, 1806-1814.
• Plumb G.W., Garcia-Conesa M.T., Kroon P.A., Rhodes M., Ridley S., Williamson G., 1999. Metabolism of chlorogenic acid by human plasma, liver, intestine and gut microflora. J. Sci. Food Agric. 79, 390-392.
• Rechner A.R., Smith M.A., Kuhnle G., Gibson G.R., Debnam E.S., Srai S.K.S., Moore K.P., Rice-Evans C.A., 2004. Colonic metabolism of dietary polyphenols: influence of structure on microbial fermentation products. Free Rad. Biol. Med. 36, 212-225.
• Rechner A.R., Pannala A.S., Rice-Evans C.A., 2001 a. Caffeic acid derivatives in artichoke extract are metabolized to phenolic acids in vivo. Free Rad. Res. 35, 195-202.
• Rechner A.R., Spencer J.P.E., Kuhnle G., Hahn U., Rice-Evans C.A., 2001 b. Novel biomarkers of the bioavailability and metabolism of caffeic acid derivatives in humans. Free Rad. Biol. Med. 30, 1213-1222.
• Rodriguez H., Landete J.M., De La Rivas B., Munoz R., 2008. Metabolism of food phenolic acids by Lactobacillusplantarum CECT 748T. Food Chem. 107, 1393-1398.
• Rondini L., Peyrat-Maillard M.N., Marsset-Baglieri A., Berset C., 2002. Sulfated ferulic acid is the main in vivo metabolite found after short-term ingestion of free ferulic acid in rats. J. Agric. Food Chem. 50, 3037-3041.
• Saija A., Tomaino A., Trombetta D., De Pasąuale A., Uccella N., Barbuzzi T., Paolino D., Bonina F., 2000. In vitro and in vivo evaluation of caffeic and ferulic acids as topical photoprotective agents. Int. J. Pharm. 199(1), 39-47.
• Scalbert A., Williamson G., 2000. Dietary intake and bioavailability of polyphenols. J. Nutr. 130, 2073S-2085S.
• Tanaka T., Kojima T., Kawamori T., Wang A., Suzui M., Okamoto K., Mori H., 1993. Inhibition of 4-nitroquinoline-l-oxide-induced rat tongue carcinogenesis by the naturally occuring plant phenolics caffeic, ellagic, chlorogenic and ferulic acids. In: Chemopreventions by plant phenolics. Oxford Univ. Press London, 1321-1325.
• Vardakou M., Palop C.N., Christakopoulos P., Faulds C.B., Gasson M.A., Narbad A., 2008. Evaluation of the prebiotic properties of wheat arabinoxylan fractions and induction of hydrolase activity in gut microflora. Int. J. Food Microbiol. 123, 166-170.
• Vardakou M., Palop C.N., Gasson M.A., Narbad A., Christakopoulos P., 2007. In vitro threestage continuous fermentation of wheat arabinoxylan fractions and induction of hydrolase activity by the gut microflora. Int. J. Biol Macromol. 41, 584-589.
• Wang X., Geng X., Egashira Y., Sanada H., 2004. Purification and characterization of a feruloyl esterase from the intestinal bacterium Lactobacillus acidophilus. Appl. Environ. Microb. 70, 2367-2372.
• Wang X., Geng X., Egashira Y., Sanada H., 2005. Release of ferulic acid from wheat bran by an inducible FAE from an intestinal bacterium Lactobacillus acidophilus. Food Sci. Technol. Res. 11,241-247.
• Yan J.-J., Cho J.-Y., Kim H.-S., Kim K.-L., Jung J.-S., Huh S.-O., Suh H.-W., Kim Y.-H., Song D.-K., 2001. Protection against (3-amyloid peptide tixicity in vivo with long-term administration of ferulic acid. Brit. J. Pharmacol. 133, 89-96.
• Young J., Wahle K.W.J., Boyle S.P., 2008. Cytoprotective effects of phenolic antioxidants and essential fatty acids in human blood monocyte and neuroblastoma celi lines: Surrogates for neurological damage in vivo. Prostag. Leukotr. Ess. 78, 145-59.
• Yuan X., Wang J., Yao H., 2005. Feruloyl oligosaccharides stimulate the growth of Bifidobacterium bifidum. Anaerobe 11, 225-229.