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Fungal Biodegradation of Tannins from Creosote Bush (Larrea Tridentata) and Tar Bush (Fluorensia Cernua) for Gallic and Ellagic Acid Production

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Fungal Biodegradation of Tannins from Creosote Bush (Larrea Tridentata) and Tar Bush (Fluorensia Cernua) for Gallic and Ellagic Acid Production J. VENTURA et al.: Fungal Biodegradation of Tannins, Food Technol. Biotechnol. 46 (2) 213–217 (2008) 213 ISSN 1330-9862 scientific note (FTB-2075) Fungal Biodegradation of Tannins from Creosote Bush (Larrea tridentata) and Tar Bush (Fluorensia cernua) for Gallic and Ellagic Acid Production Janeth Ventura1, Ruth Belmares1, Antonio Aguilera-Carbo2, Gerardo Gutiérrez-Sanchez3, Raul Rodríguez-Herrera1 and Cristóbal Noé Aguilar1* 1Food Research Department, School of Chemistry, Universidad Autónoma de Coahuila, Saltillo, MX-25 000 Coahuila, Mexico 2Department of Food Science and Nutrition, Universidad Autónoma Agraria 'Antonio Narro', Buenavista, Saltillo, MX-25 000 Coahuila, Mexico 3Complex Carbohydrate Research Center, The University of Georgia, 315 Riverband Road, GA-30602-4712 Athens, USA Received: July 11, 2006 Revised version: January 4, 2007 Accepted: June 13, 2007 Summary In the present work, the production of two potent antioxidants, gallic and ellagic acids, has been studied using solid-state fermentation (SSF) of tannin-rich aqueous plant extracts impregnated in polyurethane foam. Extracts from creosote and tar bush were ino- culated with Aspergillus niger PSH spores and impregnated in the polyurethane support. The kinetics of the fermentation was monitored every 24 h. The maximum biodegradation of hydrolysable and condensed tannins was, respectively, 16 and 42 % in creosote bush, and 40 and 83 % in tar bush. The maximal productions of gallic and ellagic acid (152 and 177 %, respectively) were reached with aqueous extracts of creosote bush. Tar bush ex- tracts inoculated with A. niger PSH spores produced only gallic acid (92 %), while ellagic acid was not recovered after the fermentation process. Results demonstrated the potential use of these plants as a source for the production of antioxidants. Key words: Aspergillus niger PSH, creosote bush, tar bush, gallic acid, ellagic acid cals and their consumption helps in the prevention of Introduction some diseases. But at high levels of consumption, they become anti-nutritional and it has been suggested that Some plant species have developed the ability to high doses induce cellular DNA damage. survive long periods of dehydration, environment with high temperature and soils poor in organic matter (1). Tannins are a large class of complex phenolic com- Plants like creosote bush (Larrea tridentata (DC.) Cov.) pounds, comprising hydrolysable, condensed and com- and tar bush (Flourensia cernua DC.) grow abundantly in plex tannins. Hydrolysable tannins are constituted of Mexican desert, but have not been exploited for use or several organic acids, such as gallic and ellagic, which application irrespective of the fact that the leaves of are usually linked by an ester-like bond with a glucose these plants contain high concentrations of tannins (2). molecule. On acidic, basic or enzymatic hydrolysis, gal- Some of these molecules are considered as nutraceuti- lotannins produce both glucose and gallic acid. On the *Corresponding author; Fax: ++52 844 4159 534; E-mail: [email protected] 214 J. VENTURA et al.: Fungal Biodegradation of Tannins, Food Technol. Biotechnol. 46 (2) 213–217 (2008) other hand, ellagitannins have one or more hexa-hydro- lated medium were used. Reactors were covered with xydiphenolic acid residues linked to glucose, forming a brown paper and incubated at 30 °C. Kinetics of the SSF diester. Their hydrolysis results in the cleavage of glu- process was monitored by collecting samples at 0, 24, 48, cose and hexa-hydroxydiphenolic residues that undergo 72 and 96 h of the process. Collected samples were spontaneous rearrangement to lactone and finally to washed using 25 mL of distilled water; and then the fer- ellagic acid (3,4). mentation liquid was recovered by compression using a Gallic acid (3,4,5-trihydroxybenzoic acid) is used in sterilized 60-mL syringe. Cotton was plugged inside the the manufacture of trimethoprim (TMP), an antibacterial syringe to avoid the passage of particles and the col- agent, in leather industry (5), and as an antioxidant (6). lected samples were stored in small plastic bottles cov- Ellagic acid has been reported to have antimutagenic, ered with aluminium foil at freezing temperature until anticarcinogenic, antioxidant, anti-viral and anti-infla- further analysis. matory activities (7–10). Several fungal strains and tan- nin-rich substrates have been used for the production of Total and hydrolysable tannins gallic acid (2,5,11). For ellagic acid, few preliminary stu- Folin-Ciocalteu method (FAO/IAEA, 2000) was used dies have been published (12). In the present paper, the for the analysis of tannins (13). In this assay, 800 mLof fermentation of the phenolic extracts of creosote bush the sample were put into a test tube and mixed with the and tar bush to produce gallic and ellagic acids during a same volume of Folin-Ciocalteu (Sigma-Aldrich) reagent, solid-state fermentation (SSF) with Aspergillus niger PSH was studied. shaken and left for 5 min. Then this solution was di- luted with 5 mL of distilled water and analyzed in a UV-Visible spectrophotometer at 725 nm for the deter- Materials and Methods mination of total tannins and at 480 nm for hydrolysable tannins. The obtained absorbance values were analyzed Plant sampling against the standard curves prepared with tannic and gallic acid for total phenols and hydrolysable tannins, Samples of creosote bush and tar bush plants were respectively. collected from February to April 2005 in the southern suburban zone of Saltillo City, Coahuila, Mexico. The collected samples were placed in black polyethylene pla- Condensed tannins stic bags and transported to the Food Research Depart- The proanthocyanidin content was evaluated as ca- ment, School of Chemistry, Universidad Autónoma de techin equivalents and analyzed by the modified HCl- Coahuila, Mexico. The leaves of both plants were sepa- -butanol method (13). Briefly, an aliquot of 0.5 mL of the rated from flowers and stems, and dried in an oven at sample was placed with 3 mL of HCl/tert-butanol (10 %, 60 °C, for a period of 7 to 10 days. After that the dried ratio 1:9), and then an aliquot of 0.1 mL of NH4Fe(SO4)2 in leaves were powdered in a mill (Mini 100, Molinos Pul- 20 % HCl was added. The mixture was sealed hermeti- vex, S.A. de C.V., Mexico), and stored in plastic bottles cally and heated for 1 h at 100 °C in a hot water bath. in a dark place. After 1 h, it was cooled and the absorbance was read at 460 nm. The catechin equivalents were calculated with Extraction of tannins reference to standard curve obtained using catechin. A mass of 100 g of dried powder was placed in an Erlenmeyer flask with 400 mL of 70 % acetone. The flask Gallic acid was covered with aluminium foil to avoid light expo- The technique reported by Sharma et al. (14) was used sure. This mixture was refluxed at 60 °C for 12 h. After for determination of gallic acid. Citrate buffer (pH=5.0), this process, the sample was filtered using Whatman fil- methanolic rhodanine 0.67 % and KOH (0.5 mol/L) ter paper no. 41 and centrifuged at 3500 rpm for 15 min. were needed for this assay and all reactants were pre-in- The solvent was removed using a rotary evaporator (Ya- cubated at 30 °C for 5 min. An aliquot of 0.5 mL was mato RE540) using a temperature below 60 °C and by mixed with 0.3 mL of methanolic rhodanine solution avoiding light exposure. and incubated under the same conditions mentioned above. After that, 0.2 mL of KOH solution were added Microorganism and inoculum and incubated again. Finally, 4 mL of distilled water Spores of Aspergillus niger PSH (DIA/UAdeC (De- were added to the reaction mixture and incubated at 30 partamento de Investigacion en Alimentos/Universidad °C for 10 min and the absorbance was read at 520 nm. Autonoma de Coahuila), Mexico collection, Mexico) were propagated on potato dextrose agar (PDA). The spores Ellagic acid were collected using Tween 80 (0.01 %). Czapek minimal The method proposed by Wilson and Hagerman (15) medium was prepared using the plant extracts as the sole was used for the determination of ellagic acid. Inside carbon source (pH=5.0). Aspergillus niger PSH spores dark test tubes 10 mg of ellagic acid or 0.1 mL of the were inoculated in this medium at a concentration of sample were placed, and then 0.1 mL of H SO (2 mol/L) 2·107 spores/mL. 2 4 were added. The test tubes were frozen at –15 °C for 10 min, then sealed and the air was removed with a sy- Culture conditions ringe. The test tubes with ellagic acid were incubated Batches of ten Erlenmeyer flasks (250 mL) with 3 g during 24 h at 100 °C. The test tubes were washed with of polyurethane foam (cubes of 0.5 cm3) sterilized and 3 mL of pyridine and filtered. For determination, to 1 impregnated (at 70 % humidity) with 7 mL of the inocu- mL of filtered sample, 1.1 mL of pyridine and 0.1 mL of J. VENTURA et al.: Fungal Biodegradation of Tannins, Food Technol. Biotechnol. 46 (2) 213–217 (2008) 215 HCl (37 %) were added, then the mixture was shaken Table 1. Kinetic evaluation of hydrolysable and condensed tan- and incubated at 30 °C for 5 min. After incubation, 0.1 nins present in aqueous phenolic extracts of creosote and tar bush mL of NaNO2 (0.01 %) was added and the absorbance was read at 538 nm. Hydrolysable tannins Time/h Creosote bush extract Tar bush extract Results and Discussion w(tannin) mg/g To evaluate antioxidant activity, the aqueous poly- phenolic extracts were used as carbon source during the 0 8.63±0.0000493 1.84±0.0000025 solid-state fermentation process using the fungal strain 24 8.00±0.0000539 1.26±0.0000435 of Aspergillus niger PSH.
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