Production of extracellular ferulic acid esterases by Lactobacillus strains using natural and synthetic carbon sources

• Autorzy: Szwajgier D. , Jakubczyk A.

Warianty tytułu

PL

Produkcja zewnątrzkomórkowych esteraz kwasu ferulowego przez szczepy z rodzaju Lactobacillus z wykorzystaniem naturalnych i syntetycznych źródeł węgla

• Języki publikacji: EN

Abstrakty

EN

Background. Ferulic acid esterases (FAE, EC 3.1.1.73), also known as feruloyl esterases, cinnamic acid esterases or cinnamoyl esterases, belong to a common group of hydrolases distributed in the plant kingdom. Especially the fungal enzymes were very well characterised in the past whereas the enzyme was rarely found in the lactic acid bacteria (LAB) strains. It is well known that strong antioxidants free phenolic acids can be released from the dietary fiber by the action of intestinal microflora composed among others also of Lactobacillus strains. The aim of this study was to examine four Lactobacillus strains (L. acidophilus KI, Z,, rhamnosus E/N, PEN, OXY) for the ability to produce extracellular FAE on different synthetic and natural carbon sources. Material and methods. The LAB strains were grown in the minimal growth media using German wheat bran, rye bran, brewers’ spent grain, isolated larchwood arabinogalactan, apple pectin, com pectin, methyl ferulate, methyl p-coumarate, methyl syringate or methyl vanillate as the sole carbon source. FAE activity was determined using the postcultivation supematants, methyl ferulate and F1PLC with UV detection. Results. The highest FAE activity was obtained with L. acidophilus KI and methyl ferulate (max. 23.34 ±0.05 activity units) and methyl p-coumarate (max. 14.96 ±0.47 activity units) as carbon sources. L. rhamnosus E/N, OXY and PEN exhibited the limited ability to produce FAE with cinnamic acids methyl esters. Methyl syringate and methyl vanillate (MS and MV) were insufficient carbon sources for FAE production. Brewers’ spent grain was the most suitable substrate for FAE production by L. acidophilus KI (max. 2.64 ±0.06 activity units) and L. rhamnosus E/N, OXY and PEN. FAE was also successfully induced by natural substrates rye bran, com pectin (L. acidophilus KI), German wheat bran and larchwood arabinogalactan (E/N, PEN) or German wheat bran and com pectin (OXY). Conclusions. This study proved the ability of Lactobacillus strains to produce FAE in the presence of a wide rangę of different ester-bound substrates. The highest enzyme activities obtained in the presence of synthetic phenolic acids methyl esters suggest that the bacteria were forced to produce FAE whereas in the presence of natural substrates other carbon sources were exploited. FAE is the enzyme of the minor importance during the de- composition of the food matrix during the intestinal absorption but the further characterisation of these enzymes should be carried on.

PL

Wstęp. Esterazy kwasu ferulowego (FAE, EC 3.1.1.73), znane jako esterazy ferulowe, esterazy cynamonowe należą do popularnej grupy hydrolaz rozpowszechnionych w królestwie roślin. W przeszłości zostały scharakteryzowane zwłaszcza grzybowe esterazy, natomiast stosunkowo rzadko był charakteryzowany enzym produkowany przez bakterie kwasu mlekowego. Wiadomo że silne przeciwutleniacze - kwasy fenolowe mogą być uwalniane z frakcji błonnika pokarmowego w wyniku działania enzymów bakterii jelitowych, w skład których wchodzą również bakterie z rodzaju Lactobacillus. Celem pracy było zbadanie czterech mikroorganizmów (L. acidophilus K1, L. rhamnosus E/N, PEN, OXY) pod kątem uzdolnień do produkcji zewnątrzkomórkowej esterazy kwasu ferulowe- go w obecności wybranych syntetycznych i naturalnych źródeł węgla. Materiał i metody. Drobnoustroje hodowano w pożywkach minimalnych z dodatkiem: otrąb z pszenicy orkisz, otrąb żytnich, wysłodzin piwowarskich, arabinogalaktanu z modrzewia, pektyn jabłkowych, pektyn kukurydzianych, ferułami metylu, p-kumaranu metylu, syringanu metylu lub wanilianu metylu jako jedynego źródła węgla. Produkcję zewnątrzkomórkowej esterazy kwasu ferulowego określano w supematantach pohodowlanych za pomocą ferulanu metylu jako substratu oraz HPLC z detekcją w zakresie UV. Wyniki. Największą aktywność esterazy kwasu ferulowego stwierdzono w supematantach po hodowli L. acidophilus KI z ferulanem metylu (maks. aktywność 23,34 ±0,05 u) i p-kumaranem metylu (maks. aktywność 14,96 ±0,47 u). L. rhamnosus E/N, OXY and PEN wykazywały ograniczoną zdolność do produkcji esterazy ferulowej w obecności metylowych pochodnych kwasów fenolowych. Nie stwierdzono obecności esterazy, gdy syringan metylu lub wanilian metylu był jedynym źródłem węgla. Wysłodziny piwowarskie były najlepszym naturalnym substratem do produkcji esterazy ferulowej przez L. acidophilus KI (maks. aktywność 2,64 ±0,06 u) i L. rhamnosus E/N, OXY and PEN. Esteraza była również produkowana gdy źródłem węgla były: otręby żytnie, pektyna kukurydziana (L. acidophilus KI), otręby z pszenicy orkisz, arabinogalaktan z modrzewia (L. rhamnosus E/N, PEN), otręby z pszenicy orkisz, pektyna kukurydziana (L. rhamnosus OXY). Wnioski. W pracy wykazano uzdolnienie bakterii z rodzaju Lactobacillus do produkcji esterazy kwasu ferulowego w obecności wielu substratów zawierających wiązania estrowe. Największe aktywności enzymatyczne uzyskane w obecności syntetycznych pochodnych kwasu ferulowego i p-kumarowego sugerują, że bakterie musiały wykorzystać to jedyne źródło węgla w formie estrowej, natomiast w obecności substratów naturalnych było możliwe wykorzystanie innych źródeł węgla. Esteraza kwasu ferulowego jest enzymem o nieco mniejszym znaczeniu w degradacji składników żywności zachodzącej w czasie trawienia jelitowego. Pomimo to wydaje się celowe dalsze charakteryzowanie omawianych enzymów produkowanych przez bakterie kwasu mlekowego.

• Wydawca: -
• Czasopismo: Acta Scientiarum Polonorum. Technologia Alimentaria
• Rocznik: 2011
• Tom: 10
• Numer: 3
• Opis fizyczny: p.287-302,fig.,ref.

Twórcy

autor

Szwajgier D.

• Department of Biotechnology, Human Nutrition and Science of Food Commodities, University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland

autor

Jakubczyk A.

Bibliografia

• 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.
• 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.
• 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.
• Boume L.C., Rice-Evans S.C., 1998. Bioavailability of ferulic acid. Biochem. Biophys. Res. Commun. 18, 253.
• Choi Y., Lee B., 2001. Culture conditions for the production of esterase from Lactobacillus casei L96. Bioproc. Biosys. Eng. 24, 59-63.
• Choudhury R., Srai K., Debnam E., Rice-Evans C.A., 1999. Urinary excretion of hy- droxycinnamates and flavonoids after orał and intravenous administration. Free Rad. Biol. Med. 27, 278-286.
• 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.
• Cuvelier M.E., Richard H., Berset C., 1992. Comparison of the antioxidative activity of some acid-phenols: structure-activity relatioship. Biosci. Biotech. Biochem. 56, 324-325.
• 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.
• GerhSuser C., 2005. Beer constituents as potential cancer chemopreventive agents. Eur. J. Cancer. 41, 1941-1954.
• Gross M., Pfeiffer M., Martini M., Campbell D., Slavin J., Potter J., 1996. The ąuantitation of metabolites of quercetin flavonols in human urine. Cancer Epidem. Biomark. Prev. 5, 711-720.
• 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 (AAPH) or Fe2+/H202: Insight into mechanisms of neuroprotection and relevance to oxidative stress-related neurodegenerative disorders. Neurochem. Int. 48 (4), 318-327.
• Kang T.W., Adesogan A.T., Kim S.C., Lee S.C., 2009. Effects of an esterase-producing inoculant on fermentation, aerobic stability, and neutral detergent fiber digestibility of com silage. J. Dairy Sci. 92 (2), 732-738.
• Kański J., Aksenova M., Stoyanova A., Butterfield D.A., 2002. Ferulic acid antioxidant protection against hydroxyl and peroxyl radical oxidation in synaptosomal and neuronal cell 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.
• Kin K.L., Lorca G.L., Gonzalez C.F., 2009. Biochemical properties of two cinnamoyl esterases purified from a Lactobacillus johnsonii strain isolated from stool samples of diabetes-resistant rats. Appl. Environ. Microbiol. 75 (15), 5018-5024.
• 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.H., Boivin P., Berset C., 1996. Antioxidant activity of barley and malt: relationship with phenolic content. Lebensm.-Wiss. u. Technol. 29, 238-244.
• Napolitano A., Costabile A., Martin-Pelaez S., Vitaglione P., Klinder A., Gibson G.R., Fogliano V., 2009. Potential prebiotic activity of oligosaccharides obtained by enzymatic conversion of durum wheat insoluble dietary fibre into soluble dietary fibre. Nutr. Metab. Cardiovas. 19, 283-290.
• 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.
• 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 Radical Bio. Med. 30,1213-1222.
• 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.
• Szwajgier D., Dmowska A., 2010. Novel ferulic acid esterases from Bifidobacterium sp. produced on selected synthetic and natural carbon sources. Acta Sci. Pol., Techol. Aliment. 9 (3), 305- -318.
• 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.
• Xiao H., Parkin K., 2007. Isolation and identification of potential cancer chemopreventive agents from methanolic extracts of green onion (Allium cepa), Phytochemistry 68, 1059-1067.
• Xiros C., Topakas E., Katapodis P., Christakopoulos P., 2008. Evaluation of Fusarium oxysporum as an enzyme factory for the hydrolysis of brewer’s spent grain with improved biodegradability for ethanol production. Ind. Crop. Prod. 28, 213-224.
• 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, 145-159.
• Yuan X., Wang J., Yao H., 2005. Feruloyl oligosaccharides stimulate the growth of Bifidobacterium bifidum. Anaerobe. 11, 225-229.
• Zeng H., Xue Y., Peng T., Shao W., 2007. Properties of xylanolytic enzyme system in bifidobacteria and their effects on the utilization of xylooligosaccharides. Food Chem. 101,1172-1177.

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