TANNASE ACTIVITY AS A CRITERION FOR THE SELECTION OF PROBIOTIC MICROORGANISMS

Main Article Content

Authors

S.A. Starovoitova

National University of Food Technologies, 68, Vladimirskaya str., Kiev, 01601, Ukraine

Abstract

Types of tannins and their sources for selection, and characteristics such as the structure and properties of the tannins, especially those of bacterial origin, were considered. The positive and negative properties of various tannins, mainly those of vegetable origin, were reviewed. The methods of biodegradation of the main types of tannins and enzymes involved in the processes of their decomposition were analysed. The possibility of using tannins and their properties in various industries, especiallyin food and pharmaceutical industries, was discussed. The data of many known researchers with respect to bacterial tannase activity and methods of determination and isolation of bacteria with tannase activity were summarized. The main tannase-producing bacteria, especially those with potential probiotic properties and use in creating bacterial drugs and functional foods (namely, bacteria that belong to the genera such asLactobacillus, Bacillus, Enterococcus,andPentococcus), were shown. Application perspectives of the tannase activity of probiotic microorganisms as a basis for pharmaceutical products-probiotics and functional foods enriched with probiotic microorganisms that have relevant antioxidant and anti-tumour properties—were discussed. The practical uses of tannase are still quite limited because of insufficient information on its properties and the complexity of its production and purification.

Keywords

tannase activity, gut microbiota, probiotics, antioxidant properties

Article Details

References

Chung K.-T., Wei C.-I., Johnson M.G. Are tannins a double-edged sword in biology and health? Trends Food Sci. Technol, 1998, vol. 9, pp. 168-175. doi: 10.1016/S0924-2244(98)00028-4.

Jiménez N., Esteban-Torres M., Mancheño J.M., et al. Tannin degradation by a novel tannase enzyme present in some Lactobacillus plantarum strains. Appl Environ Microbiol, 2014, vol. 80, no. 10, pp. 2991-2997. doi: 10.1128/AEM.00324-14.

Chávez-González M., Rodríguez-Durán L.V., Balagurusamy N., et al. Biotechnological advances and challenges of tannase: an overview. Food Bioprocess Technol., 2012, vol. 5, pp. 445-459. doi: 10.1007/s11947-011-0608-5.

Noguchi N., Ohashi T., Shiratori T., et al. Association of tannase-producing Staphylococcus lugdunensis with colon cancer and characterization of a novel tannase gene. J Gastroenterol., 2007, vol. 42, no. 5, pp. 346-351. doi: 10.1007/s00535-007-2012-5.

Iwamoto K., Tsuruta H., Nishitaini Y., Osawa R. Identification and cloning of a gene encoding tannase (tannin acylhydrolase) from Lactobacillus plantarum ATCC 14917(T). Syst. Appl. Microbiol., 2008, vol. 31, no 4, pp. 269-277. doi: 10.1016/j.syapm.2008.05.004.

Curiel J.A., Rodríguez H., Acebrón I., et al. Production and physicochemical properties of recombinant Lactobacillus plantarum tannase. J Agric Food Chem., 2009, vol. 57, no. 14, pp. 6224-6230. doi: 10.1021/jf901045s.

Sharma K.P., John P.J. Purification and characterization of tannase and tannase gene from Enterobacter sp. Process Biochem., 2011, vol. 46, pp. 240-244. doi: 10.1016/j.procbio.2010.08.016.

Ren B., Wu M., Wang Q., et al. Crystal structure of tannase from Lactobacillus plantarum. J. Mol. Biol., 2013, vol. 425, pp. 2737-2751. doi: 10.1016/j.jmb.2013.04.032.

Serrano J., Puupponen-Pimia R., Dauer A., et al. Tannins: current knowledge of food sources, intake, bioavailability and biological effects. Mol. Nutr. Food Res., 2009, vol. 53, pp. 310-329. doi: 10.1002/mnfr.200900039.

Nicholson J.K., Holmes E., Kinross J., et al. Host-gut microbiota metabolic interactions. Science, 2012, vol. 336, pp. 1262-1267. doi: 10.1126/science.1223813.

Aguilar C.N. Gutierrez-Sanchez G. Review: Sources, Properties, Applications and Potential uses of Tannin Acyl Hydrolase. Food Science and Technology International, 2001, vol. 7, no. 5, pp. 373-382. doi: 10.1106/69M3-B30K-CF7Q-RJ5G.

Khanbabaee K., Van Ree T. Tannins: Classification and definition. Natural Product Report, 2001, vol. 18, no. 6, pp. 641-649. doi: 10.1039/B101061L.

Chávez-González M., Rodríguez-Durán L.V., Balagurusamy N. et al. Biotechnological Advances and Challenges of Tannase: An Overvie. Food Bioprocess. Technol., 2012, vol. 5, pp. 445-459. doi: 10.1007/s11947-011-0608-5.

Belmares R., Contreras-Esquivel J.C., Rodriguez-Herrera R. et al. Microbial production of tannase: An enzyme with potential use in food industry. LWT Food Science and Technology, 2004, vol. 37, no. 8, pp. 857-864. doi: 10.1016/j.lwt.2004.04.002.

Aguilera-Carbó A., Augur C., Prado-Barragán L. et al. Microbial production of ellagic acid and biodegradation of ellagitannins. Applied Microbiology and Biotechnology, 2008, vol. 78, no. 2, pp. 189-199. doi: 10.1007/s00253-007-1276-2.

Joseph J.K., Abolaji J. Effect of replacing maize with graded levels of cooked Nigerian mango-seed kernals (Mangifera indica) on the performance, carcass yield and meat quality of broiler chikens. Bioresour: Technol., 1997, vol. 61, pp. 99-102. doi: 10.1016/S0960-8524(97)84705-0.

Chowdhury S.P., Khanna S., Verma S.C., Tripathi A.K. Molecular diversity of tannic acid degrading bacteria isolated from tannery soil. J. Appl. Microbiol., 2004, vol. 97, pp. 1210-1219. doi: 10.1111/j.1365-2672.2004.02426.x.

Aguilar C.N., Rodríguez R., Gutiérrez-Sánchez G. et al. Microbial tannases: advances and perspectives. Appl. Microbiol. Biotechnol., 2007, vol. 76, pp. 47-59. doi: 10.1007/s00253-007-1000-2.

Das Mohapatra P.K., Mondal K.C., Pati B.R. Tannin-an effective agent against HIV-I. In: Advances in Biotechnology. Studium, USA., 2013, pp. 419-428.

Bhat T.K., Singh B., Sharma O.P. Microbial degradation of tannins – a current perspective. Biodegradation, 1998, vol. 9, no. 5, pp. 343-357. PMID: 10192896.

Smith A.H., Zoetendal E., Mackie R.I. Bacterial mechanisms to overcome inhibitory effects of dietary tannins.Microb. Ecol., 2005, vol.50, no. 2, pp. 197-205. doi: 10.1007/s00248-004-0180-x.

Gauri S.S., Mandal S.M., Atta S., et al. Novel route of tannic acid biotransfmation and their effect on major biopolymer synthesis in Azotobacter sp. SSB81. J. Appl. Microbiol., 2012, vol. 114, no. 1, pp. 84–95. doi: 10.1111/jam.12030.

Chowdhury S.P., Khanna S., Verma S.C., Tripathi A.K. Molecular diversity of tannic acid degrading bacteria isolated from tannery soil. Journal of Applied Microbiology, 2004, vol. 97, no. 6, pp. 1210-1219. doi: 10.1111/j.1365-2672.2004.02426.x.

Nacajima H., Otani C., Niimura T. Decarboxylation of gallate by cell-free extracts of Streptococcus faecalis and Klebsiella pneumonia isolated from rat faces. Food Hygiene and Safety (ShokuhinEiseigakuZasshi), 1992, vol. 33, pp. 371-377.

Chamkha M., Patel B.C.S., Traore A., GarciaLabat J.-L.M. Isolation from a shea cake digester of a tannin-degrading Streptococcus gallolyticus strain that decarboxylates protocatechuic acid hydroxycsnnamic acid, and emendation of the species. Int. J. Syst. Evol. Microbiol., 2002, vol. 52, pp. 939-944. doi: 10.1099/00207713-52-3-939.

Osawa R., Kuroiso K., Goto S., Shimizu A. Isolation of tannin-degrading lactobacilli from humans and fermented foods. Appl. Environ. Microbiol., 2000, vol. 66, pp. 3093-3097. PMID: 10877812.

Rodríguez H., de las Rivas B., Gómez-Cordovés M.C., Muñoz R. Degradation of tannic acid by cell-free extracts of Lactobacillus plantarum. Food Chem., 2008, vol. 107, pp. 664-670. doi: 10.1016/j.foodchem.2007.08.063.

Rodríguez H., Landete J.M., de las Rivas B., Muñoz R. Metabolism of food phenolic acids by Lactobacillus plantarum CECT 748T. Food Chem., 2008, vol. 107, pp. 1393-1398. doi: 10.1016/j.foodchem.2007.09.067.

Yaoa J., Guob G.S., Renb G.H., Liu Y.H. Production, characterization and applications of tannase. Journal of Molecular Catalysis B: Enzymatic, 2014, vol. 101, pp. 137-147. doi: 10.1016/j.molcatb.2013.11.018.

Iwamoto K., Tsuruta H., Nishitaini Y., Osawa R. Identification and cloning of a gene encoding tannase (tannin acyl hydrolase) from Lactobacillus plantarum ATCC 14917 T. Syst Appl Microbiol., 2008, vol. 31, no. 4, pp. 269-277. doi: 10.1016/j.syapm.2008.05.004.

Sivashanmugam K., Jayaraman G. Production and partial purification of extra-cellular tannase by Klebsiella pneumoniae MTCC 7162 isolated from tannery effluent. Afr. J. Biotechnol., 2011, vol. 10, pp. 1364-1374. doi: 10.5897/AJB10.1209.

Jana A., Maity C., Halder S.K. et al. Structural characterization of thermostable, solvent tolerant, cytosafe tannase from Bacillus subtilis PAB2. Biochem. Eng. J., 2013, vol. 77, pp. 161-170. doi:10.1016/j.bej.2013.06.002.

Wu M., Peng X., Wen H. et al. Expression, purification, crystallization and preliminary X-ray analysis of tannase from Lactobacillus plantarum. Acta Crystallogr. F. Struct. Biol. Cryst. Commun., 2013, vol. 69, pp. 456-459. doi: 10.1107/S1744309113006143.

Wu M., Peng X., Wen H., et al. A novel low molecular weight acido-thermophilic tannase from Enterobacter cloacae MTCC 9125. Biocatal. Agric. Biotechnol., 2013, vol. 2, pp. 132-137. doi: 10.1107/S1744309113006143.

Jana A., Halder S.K., Banerjee A., et al. Biosynthesis,structural architecture and biotechnological potential of bacterial tannase: a molecularadvancement. Bioresour Technol., 2014, vol. 157, pp. 327-40. doi: 10.1016/j.biortech.2014.02.017.

Ren B., Wu M., Wang Q., et al. Crystal structure of tannase from Lactobacillus plantarum. J. Mol. Biol., 2013, vol. 425, pp. 2737-2751. doi: 10.1016/j.jmb.2013.04.032.

Matoba Y., Tanaka N., Noda M., et al. Crystallographic and mutational analyses of tannase from Lactobacillus plantarum. Proteins Struct. Funct. Bioinform., 2013, vol. 81, pp. 2052-2058. doi: 10.1002/prot.24355.

Madeira Jr. J.V., Macedo J.A., Macedo G.A. Detoxification of castor bean residues and the simultaneous production of tannase and phytase by solid-state fermentation using Paecilomyces variotii. Bioresour. Technol., 2011, vol. 102, pp. 7343-7348. doi: 10.1016/j.biortech.2011.04.099.

Lu M.J., Chu S.C., Yan L., Chen C. Effect of tannase treatment on protein-tannin aggregation and sensory attributes of green tea infusion. Food Sci. Technol., 2009, vol. 42, pp. 338-342. doi: 10.1016/j.lwt.2008.05.015.

Aithal M., Belur P.D. Enhancement of propyl gallate yield in nonaquous medium using novel cell-associated tannase of Bacillus massiliensis. Prep. Biochem. Biotechnol., 2013, vol. 43, pp. 445-455. doi: 10.1080/10826068.2012.745873.

Mondal K.C., Pati B.R. Studies on the extracellular tannase from newly isolated Bacillus licheniformis KBR 6. J. Basic Microbiol., 2000, vol. 40, pp. 223-232. doi: 10.1002/1521-4028(200008)40:4<223::AID-JOBM223>3.0.CO;2-L.

Ayed L., Hamdi M. Culture conditions of tannase production by Lactobacillus plantarum. Biotechnol. Lett., 2002, vol. 24, pp. 1763-1765. doi: 10.1023/A:1020696801584.

Sabu A., Augur C., Swati C., Pandey A. Tannase production by Lactobacillus sp. ASR-S1 under solid-state fermentation. Process Biochem., 2006, vol. 41, pp. 575-580. doi: 10.1016/j.procbio.2005.05.011.

Selwal M.K., Yadav A., Selwal K.K. et al. Optimization of cultural conditions for tannase production by Pseudomonas aeruginosa IIIB 8914 under submerged fermentation. World J. Microbiol. Biotechnol., 2010, vol. 26, pp. 599-605. doi: 10.1007/s11274-009-0209-x.

Tahmourespour A., Tabatabaee N., Khalkhali H., Amini I. Tannic acid degradation by Klebsiella strains isolated from goat feces. Iran J Microbiol., 2016, vol. 8, no. 1, pp.14-20. PMID: 27092220.

Esteban-Torres M., Landete J.M., Reverón I., et al. A Lactobacillus plantarum esterase active on a broad range of phenolic esters. Appl Environ Microbiol., 2015, vol. 81, no. 9, pp. 3235-3242. doi: 10.1128/AEM.00323-15.

López de Felipe F., de Las Rivas B., Muñoz R. Bioactive compounds produced by gut microbial tannase: implications for colorectal cancer development. Front Microbiol., 2014, vol. 5, pp. 684. doi: 10.3389/fmicb.2014.00684.

Ahrén I.L., Xu J., Önning G., et al. Antihypertensive activity of blueberries fermented by Lactobacillus plantarum DSM 15313 and effects on the gut microbiota in healthy rats. Clin Nutr., 2015, vol. 34, no. 4, pp. 719-726. doi: 10.1016/j.clnu.2014.08.009.

Zhang S., Gao X., He L., et al. Novel trends for use of microbial tannases. Prep Biochem Biotechnol., 2015, vol. 45, no. 3, pp. 221-232. doi: 10.1080/10826068.2014.907182.

Jiménez N., Curiel J.A., Reverón I., et al. Uncovering the Lactobacillus plantarum WCFS1 gallate decarboxylase involved in tannin degradation. Appl Environ Microbiol., 2013, vol. 79, no. 14, pp. 4253-4263. doi: 10.1128/AEM.00840-13.