Abstract
Tannin acyl hydrolases, also known as tannases, are a group of enzymes critical for the transformation of tannins. The study of these enzymes, which initially evolved in different organisms to detoxify and/or use these plant metabolites, has nowadays become relevant in microbial enzymology research due to their relevant role in food tannin transformation. Microorganisms, particularly bacteria, are major sources of tannase. Cloning and heterologous expression of bacterial tannase genes and structural studies have been performed in the last few years. However, a systematic compilation of the information related to all recombinant tannases, their classification, and characteristics is missing. In this review, we explore the diversity of heterologously produced bacterial tannases, describing their substrate specificity and biochemical characterization. Moreover, a new classification based on sequence similarity analysis is proposed. Finally, putative tannases have been identified in silico for each group of tannases taking advantage of the use of the “tannase” distinctive features previously proposed.
Similar content being viewed by others
References
Aguilar CN, Gutiérrez-Sánchez G (2001) Review: Sources, properties, applications and potential uses of tannin acyl hydrolase. Food Sci Technol Int 7:373–382
Aguilar CN, Rodríguez R, Gutiérrez-Sánchez G, Augur C, Favela-Torres E, Prado-Barragán LA, Ramírez-Coronel A, Contreras-Esquivel JC (2007) Microbial tannases: advances and perspectives. Appl Microbiol Biotechnol 76:47–59
Aguilar-Zárate P, Cruz-Hernández MA, Montañez JC, Belmares-Cerda RE, Aguilar CN (2014) Bacterial tannases: production, properties and applications. Rev Mex Ing Quím 13:63–74
Banerjee A, Jana A, Pati BR, Mondal KC, Das Mohapatra PK (2012) Characterization of tannase protein sequences of bacteria and fungi: an in silico study. Protein J 31:306–327. https://doi.org/10.1007/s10930-012-9405-x
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 u-Technol 37:857–864
Belur PD, Mugeraya G (2011) Microbial production of tannase: state of the art. Res J Microbiol 6:25–40
Beniwal V, Kumar A, Sharma J, Chhokar V (2013) Recent advances in industrial application of tannases: a review. Recent Pat Biotechnol 7:228–233
Benoit I, Danchin EGJ, Bleichrodt RJ, de Vries RP (2008) Biotechnological applications and potential of fungal feruloyl esterases based on prevalence, classification and biochemical diversity. Biotechnol Lett 30:387–396
Chaitanyakumar A, Anbalagan M (2016) Expression, purification and immobilization of tannase from Staphylococcus lugdunensis MTCC 3614. Appl Microb Biotech Express 6(89). https://doi.org/10.1186/s13568-016-0261-5
Chandrasekaran M, Beena PS (2013) Tannase: source, biocatalytic characteristics, and bioprocesses for production. In: Marine enzymes for biocatalysis. Chapter 11. Woodhead Publ Ltd, pp 259–293. https://doi.org/10.1533/9781908818355.3.259
Chávez-González M, Rodríguez-Durán LV, Balagurusamy N, Prado-Barragán A, Rodríguez R, Contreras JC, Aguilar CN (2012) Biotechnological advances and challenges of tannase: an overview. Food Bioprocess Technol 5:445–459
Crepin VF, Faulds CB, Connerton IF (2004) Functional classification of the microbial feruloyl esterases. Appl Microbiol Biotechnol 63:647–652
Curiel JA, Rodríguez H, Acebrón I, Mancheño JM, de las Rivas B, Muñoz R (2009) Production and physicochemical properties of recombinant Lactobacillus plantarum tannase. J Agric Food Chem 57:6224–6230. https://doi.org/10.1021/jf901045s
Curiel JA, Betancor L, de las Rivas B, Muñoz R, Guisán JM, Fernández-Lorente G (2010) Hydrolysis of tannic acid catalyzed by immobilized-stabilized derivatives of tannase from Lactobacillus plantarum. J Agric Food Chem 58:6403–6409
Deschamps AM, Mahoudeau G, Conte M, Lebeault JM (1980) Bacteria degrading tannic acid and related compounds. J Ferment Technol 58:93–97
Esteban-Torres M, Landete JM, Reverón I, Santamaría L, de las Rivas B, Muñoz R (2015) A Lactobacillus plantarum esterase active on a broad range of phenolic esters. Appl Environ Microbiol 81:3235–3242
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
Inoue KH, Hagerman AE (1988) Determination of gallotannins with rhodanine. Anal Biochem 169:363–369
Iwamoto K, Tsuruta H, Nishitaini Y, Osawa R (2008) Identification and cloning of a gene encoding tannase (tannin acylhydrolase) from Lactobacillus plantarum ATCC 14917T. Syst Appl Microbiol 31:269–277. https://doi.org/10.1016/j.syapm.2008.05.004
Jana A, Halder SK, Banerjee A, Paul T, Pati BR, Mondal KC, das Mohapatra PK (2014) Biosynthesis, structural architecture and biotechnological potential of bacterial tannase: a molecular advancement. Bioresour Technol 157:327–340. https://doi.org/10.1016/j.biortech.2014.02.017
Jiménez N, Santamaría L, Esteban-Torres M, de las Rivas B, Muñoz R (2014a) Contribution of a tannase from Atopobium parvulum DSM 20469T in the oral processing of food tannins. Food Res Int 62:397–402. https://doi.org/10.1016/j.foodres.2014.03.042
Jiménez N, Esteban-Torres M, Mancheño JM, de las Rivas B, Muñoz R (2014b) Tannin degradation by a novel tannase enzyme present in some Lactobacillus plantarum strains. Appl Environ Microbiol 80:2991–2997. https://doi.org/10.1128/AEM.00324-14
Jiménez N, Barcenilla JM, López de Felipe F, de las Rivas B, Muñoz R (2014c) Characterization of a bacterial tannase from Streptococcus gallolyticus UCN34 suitable for tannin biodegradation. Appl Microbiol Biotechnol 98:6329–6337. https://doi.org/10.1007/s00253-014-5603-0
Jiménez N, Reverón I, Esteban-Torres M, López de Felipe F, de las Rivas B, Muñoz R (2014d) Genetic and biochemical approaches towards unravelling the degradation of gallotannins by Streptococcus gallolyticus. Microb Cell Factories 13(154):154. https://doi.org/10.1186/s12934-014-0154-8
Kelly WJ, Pacheco DM, Attwood GT, Altermann E, Leahy SC (2016) The complete genome sequence of the rumen methanogen Methanobrevibacter millerae SM9. Stand Gen Sci 11(49):49. https://doi.org/10.1186/s40793-016-0171-9
Lekha PK, Lonsane BK (1997) Production and application of tannin acyl hydrolase: state of the art. Adv Appl Microb 44:212–260
Mingshu L, Kai Y, Quiang H, Dongying J (2006) Biodegradation of gallotannins and ellagitannins. J Basic Microbiol 46:68–84
Natarajan K, Rajendran A, Thangaveu V (2008) Tannase enzyme: the most promising biocatalyst for food processing industries. Biosci Biotechnol Res Asia 5:221–228
Noguchi N, Ohashi T, Shiratori T, Narui K, Hagiwara T, Ko M, Watanabe K, Miyahara T, Taira S, Moriyasu F, Sasatsu M (2007) Association of tannase-producing Staphylococcus lugdunensis with colon cancer and characterization of a novel tannase gene. J Gastroenterol 42:346–351. https://doi.org/10.1007/s00535-007-2012-5
Prasad D, Gupta RK, Mathangi G, Kamini NR, Gowthaman MK (2012) Advances in production and characteristics features of microbial tannases: an overview. Curr Trends Biotech Pharm 6:145–165
Ren B, Wu M, Wang Q, Peng X, Wen H, McKinstry WJ, Chen Q (2013) Crystal structure of tannase from Lactobacillus plantarum. J Mol Biol 425:2737–2751
Rodríguez H, de las Rivas B, Gómez-Cordovés C, Muñoz R (2008) Characterization of tannase activity in cell-free extracts of Lactobacillus plantarum CECT 748T. Int J Food Microbiol 121:92–98. https://doi.org/10.1016/jijfoodmicro.2007.11.002
Rodríguez-Durán LV, Valdivia-Urdiales B, Contreras-Esquivel JC, Rodríguez-Herrera R, Aguilar CN (2011) Novel strategies for upstream and downstream processing of tannin acyl hydrolase. Enz Res 823619:1–20. https://doi.org/10.4061/2011/823619
Serrano J, Puupponen-Pimiä R, Dauer A, Aura A-M, Saura-Calixto F (2009) Tannins: current knowledge of food sources, intake, bioavailability and biological effects. Mol Nutr Food Res 53:310–S329
Sharma KP, John PJ (2011) Purification and characterization of tannase and tannase gene from Enterobacter sp. Process Biochem 46:240–244. https://doi.org/10.1016/j.procbio.2010.08.016
Suzuki K, Hori A, Kawamoto K, Thangudu RR, Ishida T, Igarashi K, Samejima M, Yamada C, Arakawa T, Wakagi T, Koseki T, Fushinobu S (2014) Crystal structure of a feruloyl esterase belonging to the tannase family: a disulphide bond near a catalytic triad. Proteins 82:2857–2867
Tomás-Cortázar J, Plaza-Vinuesa L, de las Rivas B, Lavin JL, Barriales D, Abecia L, Mancheño JM, Aransay AM, Muñoz R, Anguita J, Rodríguez H (2018) Identification of a highly active tannase enzyme from the oral pathogen Fusobacterium nucleatum subsp. polymorphum. Microb Cell Factories 17:33. https://doi.org/10.1186/s12934-018-0880-4
Ueda S, Nomoto R, Yoshida K, Osawa R (2014) Comparison of three tannases cloned from closely related Lactobacillus species: L. plantarum, L. paraplantarum, and L. pentosus. Microb Cell Fact 14:87. https://doi.org/10.1186/1471-2180-14-87
Wu M, Peng X, Wen H, Wang Q, Chen Q, McKinstry WJ, Reb B (2013) Expression, purification, crystallization and preliminary X-ray analysis of tannase from Lactobacillus plantarum. Acta Crystallogr Scet F: Struc Biol Cryst Commun 69:456–459
Wu M, Wang Q, McKinstry WJ, Ren B (2015) Characterization of a tannin acyl hydrolase from Streptomyces sviceus with substrate preference for digalloyl ester bonds. Appl Microbiol Biotechnol 99:2663–2672. https://doi.org/10.1007/s00253-014-6085-9
Yao J, Fan XJ, Liu YH (2011) Isolation and characterization of a novel tannase from a metagenomic library. J Agric Food Chem 59:3812–3818. https://doi.org/10.1021/jf104394m
Yao J, Chen QL, Shen AX, Liu YH (2013) A novel feruloyl esterase from a soil metagneomic library with tannase activity. J Mol Catal B Enzym 95:55–61
Yao J, Guo GS, Ren GH, Liu YH (2014a) Production, characterization and applications of tannase. J Mol Catal B Enzym 101:137–147
Yao J, Chen Q, Zhong G, Cao W, Yu A, Liu Y (2014b) Immobilization and characterization of tannase from a metagenomics library and its use for removal of tannins from green tea infusion. J Microbiol Biotechnol 24:80–86
Zhang S, Gao X, He L, Qiu Y, Zhu H, Cao Y (2015) Novel trends for use of microbial tannases. Prep Biochem Biotechnol 45:221–232. https://doi.org/10.1080/10826068.2014.907182
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
Acknowledgements
We thank MINEICO for the Severo Ochoa Excellence accreditation (SEV-2016-0644).
Funding
This work was financially supported by grants AGL2014-52911-R and SAF2015-73549-JIN from the Spanish Ministry of Economy and Competitiveness/FEDR-MINEICO.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical statement
This article does not contain any studies with human participants or animal performed by any of the authors.
Electronic supplementary material
ESM 1
(PDF 806 kb)
Rights and permissions
About this article
Cite this article
de las Rivas, B., Rodríguez, H., Anguita, J. et al. Bacterial tannases: classification and biochemical properties. Appl Microbiol Biotechnol 103, 603–623 (2019). https://doi.org/10.1007/s00253-018-9519-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-018-9519-y