Abstract
In the last years, tannase has been the subject of a lot of studies due to its commercial importance and complexity as catalytic molecule. Tannases are capable of hydrolyzing complex tannins, which represent the main chemical group of natural anti-microbials occurring in the plants. The general outline of this work includes information of the substrates, the enzyme, and the applications. This review considers in its introduction the concepts and history of tannase and explores scientific and technological aspects. The “advances” trace the route from the general, molecular, catalytic, and functional information obtained under close to optimal conditions for microbial production through purification, description of the enzyme properties, and the commercial applications to the “perspectives” including expression studies, regulation, and potential uses; aspects related to the progress in our understanding of tannin biodegradation are also included.
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References
Abdel-Naby MA, Sherif AA, El-Tanash AB, Mankarios AT (1999) Immobilization of Aspergillus oryzae tannase and properties of the immobilized enzyme. J Appl Microbiol 87:108–114
Adachi O, Watanabe M, Yamada H (1971) Physicochemical properties of the tannase from Aspergillus flavus. Agric Biol Chem 32:1079–1085
Aguilar CN, Augur C, Favela-Torres E, Viniegra-González G (2001a) Induction and repression patterns of fungal tannase in solid-state and submerged cultures. Proc Biochem 36:565–570
Aguilar CN, Augur C, Favela-Torres E, Viniegra-González G (2001b) Production of tannase by Aspergillus niger Aa-20 in submerged and solid state fermentation: influence of glucose and tannic acid. J Ind Microbiol Biotechnol 26:296–302
Aguilar CN, Augur C, Viniegra-González G, Favela-Torres E (1999) A comparison of methods to determine tannin acyl hydrolase activity. Braz Arch Biol Technol 42:355–361
Aguilar CN, Favela-Torres E, Viniegra-González G, Augur C (2002) Culture conditions dictate protease and tannase production in submerged and solid-state cultures by Aspergillus niger Aa-20. Appl Biochem Biotechnol 102–103:407–414
Aguilar CN, Gutiérrez-Sánchez G (2001) Review sources, properties, applications and potential uses of tannin acyl hydrolase. Food Sci Technol Int 7:373–382
Albertse EK (2002) Cloning, expression and characterization of tannase from Aspergillus species. M.Sc. thesis, Faculty of Natural and Agricultural Sciences, Department of Microbiology and Biotechnology, University of the Free State Bloemfontein, South Africa
Aoki K, Shinke R, Nishira H (1976) Purification and some properties of yeast tannase. Agric Biol Chem 40:79–85
Ayed L, Hamdi M (2002) Culture conditions of tannase production by Lactobacillus plantarum. Biotechnol Lett 24:1763–1765
Bajpai B, Patil S (1997) Introduction of tannin acyl hydrolase (EC 3.1.1.20) activity in some members of fungi imperfecti. Enzyme Microb Technol 20:612–614
Banerjee D, Mondal K, Bikas R (2001) Production and characterization of extracellular and intracellular tannase from newly isolated Aspergillus aculeatus DBF9. J Basic Microbiol 6:313–318
Banerjee R, Mukherjee G, Patra KC (2005) Microbial transformation of tannin-rich substrate to gallic acid through co-culture method. Bioresour Technol 96:949–953
Barthomeuf C, Regerat F, Pourrat H (1994) Production, purification and characterization of tannase from Aspergillus niger LCF8. J Ferment Technol 77:137–142
Batra A, Saxena RK (2005) Potential tannase producers from the genera Aspergillus and Penicillium. Proc Biochem 40:1553–1557
Battestin V, Alves-Macedo G (2007) Tannase production by Paecilomyces variotii. Bioresour Technol 98:1832–1837
Belmares R, Contreras-Esquivel JC, Rodríguez-Herrera R, Ramírez Coronel A, Aguilar CN (2004) Microbial production of tannase: an enzyme with potential use in food industry. Lebensm Wiss Technol 37:857–864
Bhat TK, Singh B, Sharma OP (1998) Microbial degradation of tannins. A current perspective. Biodegradation 9:343–357
Boadi DK, Neufeld RJ (2001) Encapsulation of tannase for the hydrolysis of tea tannins. Enzyme Microb Technol 28:590–595
Bradoo S, Gupta R, Saxena RK (1997) Parametric optimization and biochemical regulation of extracellular tannase from Aspergillus japonicus. Proc Biochem 32:135–139
Bradoo S, Gupta R, Saxena R (1996) Screening of extracellular tannase producing fungi: development of a rapid simple plate assay. J Gen Appl Microbiol 42:325–329
Cerda-Gomez A, Contreras-Esquivel JC, Reyes-Valdes H, Rodríguez R, Aguilar CN (2006) Molecular characterization of Aspergillus strains producers of tannase. Proceedings of the second international congress on food science and technology in developing countries, Saltillo, Coahuila, Mexico (FEMB-18)
Chae S, Yu T (1983) Experimental manufacture of a com wine by fungal tannase. Hanguk Sipkum Kwahakoechi 15:326–332
Chang FS, Chen PC, Chen RC, Lu FM, Cheng TJ (2006) Real-time assay of immobilized tannase with a stopped-flow conductometric device. Bioelectrochemistry 69:113–116
Chaterjee R, Dutta A, Banerjee R, Bhattacharyya BC (1996) Production of tannase by solid state fermentation. Bioprocess Eng 14:159–162
Coggon P, Graham NH, Sanderson GW (1975) UK Patent 1,380,135
Contreras-Dominguez M, Guyot S, Marnet N, Le Petit J, Perraud-Gaime I, Roussos S, Augur C (2006) Degradation of procyanidins by Aspergillus fumigatus: identification of a a novel aromatic ring cleavage product. Biochimie 88:1899–1908
Cruz-Hernández M, Augur C, Rodríguez R, Contreras-Esquivel J, Aguilar CN (2006) Evaluation of culture conditions for tannase production by Aspergillus niger GH1. Food Technol Biotechnol 44:541–544
Deschamps AM, Otuk G, Lebeault JM (1983) Production of tannase and degradation of chestnut tannin by bacteria. J Ferment Technol 61:55–59
Dueñas M, Hernández T, Estrella I (2007) Changes in the content of bioactive polyphenolic compounds of lentils by the action of exogenous enzymes. Effect on their antioxidant activity. Food Chem 101:90–97
Farias GM, Gorbea C, Elkins JR, Griffin GJ (1994) Purification, characterization, and substrate relationships of the tannase from Cryphonectria parasitica. Physiol Mol Plant Pathol 44:51–63
Gaathon A, Gross Z, Rozhanski M (1989) Propyl gallate: enzymatic synthesis in a reverse micelle system. Enzyme Microb Technol 11:604–609
Gammoun A, Moros J, Tahiri S, Garriques S, Guardia M (2006) Partial least-squares near-infrared determination of hydrocarbons removed from polluted waters by tanned solid wastes. Anal Bioanal Chem 385:766–770
Ganga PS, Nandy SC, Santappa M (1977) Effect of environmental factors on the production of fungal tannase. Leather Sci 24:8–16
García-Conesa MT, Ostergaard P, Kauppinen S, Williamson G (2001) Hydrolysis of diethyl diferulates by a tannase from Aspergillus oryzae. Carbohydr Polym 44:319–324
García-Nájera JA, Contreras-Esquivel JC, Rodríguez-Herrera R, Prado-Barragan LA, Aguilar CN (2002) Fungal production of 3,4,5-trihydroxybenzoic acid in submerged culture (in Spanish). Proceedings of the third international symposium on bioprocess engineering, IBT-UNAM, Cuernavaca, Morelos, Mexico
García-Peña I (1996) Production and characterization of a tannase produced by Aspergillus níger in solid state culture (in Spanish). M.Sc. thesis, Universidad Autónoma Metropolitana, Iztapalapa, Mexico
García-Peña I, Augur C, Favela-Torres E (1999) Partial purification of Aspergillus niger tannase produced by solid state culture (in Spanish). In: Prado A, Huerta S, Rodríguez G, Sancedo G (eds) Advances in enzyme purification and applied biotechnology. Ediciones UAM-Iztapalapa, Mexico, DF, pp 247–261, 2207–2212
Goel G, Puniya AK, Aguilar CN, Singh K. (2005) Interaction of gut microflora with tannins in feeds. Naturwissenschaften 92:497–503
Goel G, Puniya AK, Singh K (2007) Phenotypic characterization of tannin–protein complex degrading bacteria from faeces of goat. Small Rumin Res 69:217–220
Hadi TA, Banerjee R, Bhattarcharyya BC (1994) Optimization of tannase biosynthesis by a newly isolated Rhizopus oryzae. Bioprocess Eng 11:239–243
Hatamoto O, Watarai T, Kikuchi M, Mizusawa K, Sekine H (1996) Cloning and sequencing of the gene encoding tannase and a structural study of the tannase subunit from Aspergillus oryzae. Gene 175:215–221
Hatamoto O, Watarai T, Kikuchi M, Mizusawa K, Sekine H (1997) Erratum to: ‘cloning and sequencing of the gene encoding tannase and a structural study of the tannase subunit from Aspergillus oryzae’ [Gene 175 (1996) 215–221]. Gene 186:1–153
Huang W, Ni J, Borthwick AGL (2005) Biosynthesis of valonia tannin hydrolase and hydrolysis of valonia tannin to ellagic acid by Aspergillus SHL 6. Process Biochem 40:1245–1249
Ibuchi S, Minoda Y, Yamada K (1972) Hydrolyzing pathway, substrate specificity and inhibition of tannin acyl hydrolase. Agric Biol Chem 32:803–809
Kar B, Banerjee R (2000) Biosynthesis of tannin acyl hydrolase from tannin rich forest residue under different fermentation conditions. J Ind Microbiol Biotechnol 25:29–38
Kar B, Banerjee R, Bhattacharyya BC (2002) Optimization of physicochemical parameters for gallic acid production by evolutionary operation-factorial design technique. Process Biochem 37:1395–1401
Kar B, Banerjee R, Bhattacharyya BC (2003) Effect of additives on the behavioural properties of tannin acyl hydrolase. Process Biochem 38:1285–1293
Kostinek M, Specht I, Edward VA, Pinto C, Egounlety M, Sossa C, Mbugua S, Dortu C, Thonart P, Taljaard L (2007) Characterisation and biochemical properties of predominant lactic acid bacteria from fermenting cassava for selection as starter cultures. Int J Food Microbiol 114:342–351
Kumar R, Sharma J, Singh R (2006) Production of tannase from Aspergillus ruber under solid state fermentation using jamun (Syzygium cumini) leaves. Microbiol Res (in press).DOI https://doi.org/10.1016/J.micres.2006.06.012
Lee J, Talcott ST (2005) Enzyme hydrolysis of ellagic acid derivatives in muscadine grapes (Vitis rotundifolia). Session 36E, fruit and vegetable products: general. IFT annual meeting, July 15–20, New Orleans, La, USA
Lekha PK, Lonsane BK (1997) Production and application of tannin acyl hydrolase: state of the art. Adv Appl Microbiol 44:215–260
Lekha P, Lonsane B (1994) Comparative titres, location and properties of tannin acyl hydrolase produced by Aspergillus niger PKL 104 in solid-state, liquid surface and submerged fermentations. Process Biochem 29:497–503
Lekha P, Ramakrishna M, Lonsane B (1993) Strategies for isolation of potent culture capable of producing tannin acyl hydrolase in higher titres. Chem Mikrobiol Technol Lebensm 15:5–10
Lewis JA, Starkey RL (1969) Decomposition of plant tannins by some soil microorganisms. Soil Sci 107:235–241
López-Ríos GF (1984) Fitoquímica, 1st edn. Universidad Autónoma de Chapingo, Estado de México, p 13
Mahapatra K, Nanda RK, Bag SS, Banerjee R, Pandey A, Szakacs G (2005) Purification, characterization and some studies on secondary structure of tannase from Aspergillus awamori nakazawa. Process Biochem 40:3251–3254
Mahendran B, Raman N, Kim D (2005) Purification and characterization of tannase from Paecilomyces variotii: hydrolysis of tannic acid using immobilized tannase. Appl Microbiol Biotechnol 70:445–451
Mendez A (1984) Energía metabolizable del sorgo y efecto de la adición de aceite a dietas con sorgo dulce o amargo. Avances de investigación (resumenes), Colegio de Postgraduados
Mingshu L, Kai Y, Qiang H, Dongying J (2006) Biodegradation of gallotannins and ellagitannins. J Basic Microbiol 46:68–84
Mondal K, Banerjee D, Banerjee R, Pati B (2001b) Production and characterization of tannase from Bacillus cereus KBR9. J Gen Appl Microbiol 47:263–267
Mondal K, Samanta S, Giri S, Pati B (2001a) Distribution of tannic acid degrading microorganisms in the soil and comparative study of tannase from two fungal strains. Acta Microbiol Pol 50:75–82
Mukherjee G, Banerjee R (2005) Effects of temperature, pH and additives on the activity of tannase produced by a co-culture of Rhizopus oryzae and Aspergillus foetidus. World J Microbiol Biotechnol 22:207–211
Murugan K, Saravanababu S, Arunachalam M (2007) Screening of tannin acyl hydrolase (E.C.3.1.1.20) producing tannery effluent fungal isolates using simple agar plate and SmF process. Bioresour Technol 98:946–949
Nip WK, Burns EE (1969) Pigment characterization in grain sorghum, I. Red varieties. Cereal Chem 46:490–495
Nishitani Y, Osawa R (2003) A novel colorimetric method to quantify tannase activity of viable bacteria. J Microbiol Methods 54:281–284
Nishitani Y, Sasaki E, Fujisawa T, Osawa R (2004) Genotypic Analyses of Lactobacilli with a range of tannase activities isolated from human feces and fermented foods. Syst Appl Microbiol 27:109–117
Nuero OM, Reyes F (2002) Enzymes for animal feeding from Penicillium chrysogenum mycelial wastes from penicillin manufacture. Lett App Microbiol 34:413–416
Pinto G, Bruno L, Hamacher M, Tarzi S, Couri S (2003) Increase of tannase production in solid state fermentation by Aspergillus niger 3T5B8. 25th Symposium on biotechnology for fuels and chemicals, poster presentation, Breckenridge, CO, USA, pp 3–68
Pinto G, Couri S, Goncalves E (2006) Replacement of methanol by ethanol on gallic acid determination by rhodanine and its impacts on the tannase assay. EJEAFCHe 5:5. http://ejeafche.uvigo.es/5(5)2006/009552006F.htm
Pinto G, Leite S, Tarzi S, Couri S (2001) Selection of tannase-producing Aspergillus niger strains. Braz J Microbiol 32:24–26
Pourrat H, Regerat F, Pourrat A, Jean D (1985) Production of gallic acid from tara tannin by a strain of A. niger. J Ferment Technol 63:401–403
Purohit JS, Dutta JR, Nanda RK, Banerjee R (2006) Strain improvement for tannase production from coculture of Aspergillus foetidus and Rhizopus oryzae. Bioresour Technol 97:795–801
Raab T, Bel-Rhlid R, Williamson G, Hansen CE, Chaillot D (2007) Enzymatic galloylation of catechins in room temperature ionic liquids. J Mol Catal B Enzym 44:60–65
Rajkumar GS, Nandy SC (1983) Isolation purification and some properties of Penicillium chrysogenum tannase. Appl Environ Microbiol 46:525–527
Ramirez-Coronel A, Marnet N, Kumar V, Rousses S, Guyot S, Augur C (2004) Characterization and estimation of proanthocyanidins and other phenolics in coffee pulp (Coffea arabica) by thiolysis-high-performance liquid chromatography. J Agric Food Chem 52:1344–1349
Ramírez-Coronel A, Viniegra-González G, Augur C (1999) Purification of a tannase produced by Aspergillus niger Aa-20, in solid state fermentation. Proceedings of the VIII Mexican congress and IV Latin American congress of biotechnology and bioengineering, Huatulco, Oaxaca, Mexico
Ramirez-Coronel MA, Viniegra-Gonzalez G, Darvill A, Augur C (2003) A novel tannase from Aspergillus niger with β-glucosidase activity. Microbiology 149:2941–2946
Rana N, Bhat T (2005) Effect of fermentation system on the production and properties of tannase of Aspergillus niger van Tieghem MTCC 2425. J Gen Appl Microbiol 51:203–212
Rout S, Banerjee R (2006) Production of tannase under mSSF and its application in fruit juice debittering. Ind J Biotechnol 5:351–356
Saavedra G, Couri S, Ferreira S, Sousa de Brito E (2005) Tannase: conceitos, producto e aplicacao (in Portuguese). B.CEPPA Curitiba 23:435–462
Sabu A, Pandey A, Jaafar Daud M, Szakacs G (2005) Tamarind seed powder and palm kernel cake: two novel agro residues for the production of tannase under solid state fermentation by Aspergillus niger ATCC 16620. Bioresour Technol 96:1223–1228
Sabu A, Augur C, Swati C, Pandey A (2006) Tannase production by Lactobacillus sp. ASR-S1 under solid-state fermentation. Process Biochem 41:575–580
Sanchez EE (2001) Applications and potential uses of tannase and tannins (in Spanish). B.Sc. thesis, Universidad Autónoma de Coahuila, Saltillo, Coah, p 25
Sasaki E, Shimada T, Osawa R, Nishitani Y, Spring S, Lang E (2005) Isolation of tannin-degrading bacteria isolated from feces of the Japanese large wood mouse, Apodemus speciosus, feeding on tannin-rich acorns. Syst Appl Microbiol 28:358–365
Scalbert A (1991) Antimicrobial properties of tannins. Phytochemistry 30:3875–3883
Sharma S, Gupta MN (2003) Synthesis of antioxidant propyl gallate using tannase from Aspergillus niger van Teighem in nonaqueous media. Bioorg Med Chem Lett 13:395–397
Sharma S, Bhat TK, Gupta MN (2002) Bioaffinity immobilization of tannase from Aspergillus niger on concavalin A-sepharose CL-4B. Biotechnol Appl Biochem 35:165–169
Shi B, He Q, Yao K, Huang W, Li Q (2005) Production of ellagic acid from degradation of valonea tannins by Aspergillus niger and Candida utilis. J Chem Technol Biotechnol 80:1154–1159
Sittig M (1988) Trimethoprim. In: Sittig M (ed) Pharmaceutical manufacturing encyclopedia. William Andrew/Noyes, New Jersey, pp 282–284
Tieghem, P (1867) Sur la fermentation gallique. CR Acad Sci (Paris) 65:1091–1094
Treviño-Cueto B, Luis M, Contreras-Esquivel JC, Rodríguez R, Aguilera A, Aguilar CN (2007) Gallic acid and tannase accumulation during fungal solid state culture of a tannin-rich desert plant (Larrea tridentate Cov). Bioresour Technol 98:721–724
Van de Lagemaat J, Pyle DL (2001) Solid-state fermentation and bioremediation: development of a continuous process for the production of fungal tannases. Chem Eng J 84:115–123
Van de Lagemaat J, Pyle DL (2005) Modelling the uptake and growth kinetics of Penicillium glabrum in a tannic acid-containing solid-state fermentation for tannase production. Process Biochem 40:1773–1782
Van Diepeningen AD, Debet A, Varga J, Van der Gaag M, Swart K, Hoekstra R (2004) Efficient degradation of tannic acid by black Aspergillus species. Mycol Res 108:919–925
Vaquero I, Marcobal A, Muñoz R (2004) Tannase activity by lactic acid bacteria isolated from grape must and wine. Int J Food Microbiol 96:199–204
Vattem DA, Shetty K (2002) Solid-state production of phenolic antioxidants from cranberry pomace by Rhizopus oligosporum. Food Biotechnol 16:189–210
Vattem DA, Shetty K (2003) Ellagic acid production and phenolic antioxidants activity in cranberry pomace (Vaccinium macrocarpo) mediated by Lentinus edodes using a solid-state system. Process Biochem 39:367–379
Viniegra-González G, Favela-Torres E, Aguilar CN, Rómero-Gomez SJ, Díaz-Godínez G, Augur C (2003) Advantages of fungal enzyme production in solid state over liquid fermentation systems. Biochem Eng J 13:157–167
Vivas N, Laguerrre M, Pianet de Boissel I, Vivas de Gaulejac N, Nonier MF (2004) Conformational interpretation of vascalagin and castalagin physicochemical properties. J Agric Food Chem 52:2073–2078
Yamada K, Iibuchi S, Minoda Y (1968) Studies on tannin acyl hydrolase of microorganisms. Isolation and identification of producing molds and studies on the conditions of cultivation. Agric Biol Chem 45:233–240
Yoshida T, Amakura Y, Koyura N, Ito H, Isaza JH, Ramírez S, Peláez DP, Renner SS (1999) Oligomeric hydrolysable tannins from Tibouchina multiflora. Phytochemistry 52:1661–1666
Yu X, Li Y, Wu D (2004) Enzymatic synthesis of gallic acid esters using microencapsulated tannase: effect of organic solvents and enzyme specificity. J Mol Catal B Enzym 30(2):69–73
Yu XW, Li YQ (2006) Kinetics and thermodynamics of synthesis of propyl gallate by mycelium-bound tannase from Aspergillus niger in organic solvent. J Mol Catal B Enzym 40:44–50
Zhang YJ, Abe T, Tanaka T, Yang CR, Kouna I (2001) Phyllanemblinins A–F, new ellagitannins from Phyllanthus emblica. J Nat Prod 64:1527–1532
Zhong X, Peng L, Zheng S, Sun Z, Ren Y, Dong M, Xu A (2004) Secretion, purification, and characterization of a recombinant Aspergillus oryzae tannase in Pichia pastoris. Protein Expr Purif 36:165–169
Acknowledgment
C. N. Aguilar thanks CONACYT–SEP (project no. 42244) and COAH–CONACYT (COAH-2002-CO1.2565 and 4652) for financial support. The present work was conducted within the framework of the ECOS program (M02A02, project between Mexico–France).
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Aguilar, C.N., Rodríguez, R., Gutiérrez-Sánchez, G. et al. Microbial tannases: advances and perspectives. Appl Microbiol Biotechnol 76, 47–59 (2007). https://doi.org/10.1007/s00253-007-1000-2
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DOI: https://doi.org/10.1007/s00253-007-1000-2