Applied Microbiology and Biotechnology

, Volume 102, Issue 24, pp 10361–10375 | Cite as

Biotransformation of industrial tannins by filamentous fungi

  • Valeria Prigione
  • Federica Spina
  • Valeria Tigini
  • Samuele Giovando
  • Giovanna Cristina VareseEmail author


Tannins are secondary metabolites that are widely distributed in the plant kingdom. They act as growth inhibitors for many microorganisms: they are released upon microbial attack, helping to fight infection in plant tissues. Extraction of tannins from plants is an active industrial sector with several applications, including oenology, animal feeding, mining, the chemical industry, and, in particular, the tanning industry. However, tannins are also considered very recalcitrant pollutants in wastewater of diverse origin. The ability to grow on plant substrates rich in tannins and on industrial tannin preparations is usually considered typical of some species of fungi. These organisms are able to tolerate the toxicity of tannins thanks to the production of enzymes that transform or degrade these substrates, mainly through hydrolysis and oxidation. Filamentous fungi capable of degrading tannins could have a strong environmental impact as bioremediation agents, in particular in the treatment of tanning wastewaters.


Industrial tannins Filamentous fungi Tannery wastewater Biotransformation Bioremediation Laccases 



The authors are grateful to Dr. Daniel Edward Chamberlain for the revision of English.

Compliance with ethical standards

This article does not contain any studies with human participants performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abdel-Naby MA, El-Tanash AB, Sherief ADA (2016) Structural characterization, catalytic, kinetic and thermodynamic properties of Aspergillus oryzae tannase. Int J Biol Macromol 92:803–811. CrossRefPubMedGoogle Scholar
  2. Aguilar CN, Augur C, Favela-Torres E, Viniegra-González G (2001) 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. CrossRefPubMedGoogle Scholar
  3. Aguilar CN, Rodriguez R, Gutierrez-Sanchez G, Augur C, Favela-Torres E, Prado-Barragan LA, Ramirez-Coronel A, Contreras-Esquivel JC (2007) Microbial tannases: advances and perspectives. Appl Microbiol Biotechnol 76:47–59. CrossRefPubMedGoogle Scholar
  4. Aguilera-Carbo A, Augur C, Prado-Barragan LA, Favela-Torres E, Aguilar CN (2008) Microbial production of ellagic acid and biodegradation of ellagitannins. Appl Microbiol Biotechnol 78:189–199. CrossRefPubMedGoogle Scholar
  5. Aissam H, Errachidi F, Penninckx MJ, Merzouki M, Benlemlih M (2005) Production of tannase by Aspergillus niger HA37 growing on tannic acid and olive mill waste waters. World J Microbiol Biotechnol 21:609–614. CrossRefGoogle Scholar
  6. Akhtar S, Ismail T, Fraternale D, Sestili P (2015) Pomegranate peel and peel extracts: chemistry and food features. Food Chem 174:417–425. CrossRefPubMedGoogle Scholar
  7. Arca-Ramos A, Eibes G, Feijoo G, Jm L, Moreira MT (2018) Enzymatic reactors for the removal of recalcitrant compounds in wastewater. Biocatal Biotransform 36(3):195–215. CrossRefGoogle Scholar
  8. Badia-Fabregat M, Lucas D, Tuomivirta T, Fritze H, Pennanen T, Rodriguez-Mozaz S, Barcel D, Caminal G, Vicent T (2017) Study of the effect of the bacterial and fungal communities present in real wastewater effluents on the performance of fungal treatments. Sci Total Environ 579:366–377. CrossRefPubMedGoogle Scholar
  9. Baik JH, Suh HJ, Cho SY, Park Y, Choi H-S (2014) Differential activities of fungi-derived tannases on biotransformation and substrate inhibition in green tea extract. J Biosci Bioeng 118(5):546–553. CrossRefPubMedGoogle Scholar
  10. Bains G, Kumar AS, Rudrappa T, Alff E, Hanson TE, Bais HP (2009) Native plant and microbial contributions to a negative plant-plant interaction. Plant Physiol 151:2145–2151. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bajpai B, Patil S (1996) Tannin acyl hydrolase activity of Aspergillus, Penicillium, Fusarium and Trichoderma. World J Microbiol Biotechnol 12:217–220. CrossRefPubMedGoogle Scholar
  12. Bajpai B, Patil S (1997) Introduction of tannin acyl hydrolase (EC activity on some members of fungi imperfecti. Enzym Microb Technol 20:612–614CrossRefGoogle Scholar
  13. 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. CrossRefGoogle Scholar
  14. Bardi A, Yuan Q, Siracusa G, Chicca I, Islam M, Spennati F, Tigini V, Di Gregorio S, Levin DB, Petroni G, Munz G (2017a) Effect of cellulose as co-substrate on old landfill leachate treatment using white-rot fungi. Bioresour Technol 241:1067–1076. CrossRefPubMedGoogle Scholar
  15. Bardi A, Yuan Q, Tigini V, Spina F, Varese GC, Spennati F, Becarelli S, Di Gregorio S, Petroni G, Munz G (2017b) Recalcitrant compounds removal in raw leachate and synthetic effluents using the white-rot fungus Bjerkandera adusta. Water 9:824. CrossRefGoogle Scholar
  16. Batra A, Saxena RK (2005) Potential tannase producers from the genera Aspergillus and Penicillium. Process Biochem 40:1553–1557. CrossRefGoogle Scholar
  17. Battestin V, Alves-Macedo G (2007) Tannase production by Paecilomyces variotii. Bioresour Technol 98:1832–1837. CrossRefPubMedGoogle Scholar
  18. Beena PS, Basheer SM, Bhat SG, Bahkali AH, Chandrasekaran M (2011) Propyl gallate synthesis using acidophilic tannase and simultaneous production of tannase and gallic acid by marine Aspergillus awamori BTMFW032. Appl Biochem Biotechnol 164:612–628. CrossRefPubMedGoogle Scholar
  19. Belmares R, Contreras-Esquivel JC, Rodriguez-Herrera R, Ramirez Coronel A, Aguilar CN (2004) Microbial production of tannase: an enzyme with potential use of food industry. LWT-Food Sci Technol 37:857–864. CrossRefGoogle Scholar
  20. Bhat TK, Singh B, Sharma OP (1998) Microbial degradation of tannins – a current perspective. Biodegradation 9:343–357. CrossRefPubMedGoogle Scholar
  21. Bhoite RN, Murthy PS (2015) Biodegradation of coffee pulp tannin by Penicillium verrucosum for production of tannase, statistical optimization and its application. Food Bioprod Process 94:727–735. CrossRefGoogle Scholar
  22. Böer E, Bode R, Mock H-P, Piontek M, Kunze G (2009) Atan1p — an extracellular tannase from the dimorphic yeast Arxula adeninivorans: molecular cloning of the ATAN1 gene and characterization of the recombinant enzyme. Yeast 26:323–337. CrossRefPubMedGoogle Scholar
  23. Bradoo S, Gupta R, Saxena R (1996) Screening of extracellular tannase producing fungi: development of rapid simple plate assay. J Gen Appl Microbiol 42:325–329CrossRefGoogle Scholar
  24. Bressan Gonçalves H, Jorge JA, Costa Pessela B, Fernandez Lorente G, Guisan JM, Souza Guimaraes LH (2013) Characterization of a tannase from Emericela nidulans immobilized on ionic and covalent supports for propyl gallate synthesis. Biotechnol Lett 35:591–598. CrossRefGoogle Scholar
  25. Cabral LD, Pinto VF, Patriarca A (2013) Application of plant derived compounds to control fungal spoilage and mycotoxin production in foods. Int J Food Microbiol 166:1–14. CrossRefGoogle Scholar
  26. Chambergo FS, Valencia EY (2016) Fungal biodiversity to biotechnology. Appl Microbiol Biotechnol 100:2567–2577. CrossRefPubMedGoogle Scholar
  27. Chaudhary P, Chhokar V, Kumar A, Beniwal V (2017) Bioremediation of tannery wastewater. In: Kumar R, Sharma A, Ahluwalia S (eds) Advances in environmental biotechnology. Springer, Singapore, pp 125–144CrossRefGoogle Scholar
  28. 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. CrossRefGoogle Scholar
  29. Crestini C, Lange H (2015) A novel and efficient immobilised tannase coated by the layer-by-layer technique in the hydrolysis of gallotannins and ellagitannins. Microchem J 123:139–147. CrossRefGoogle Scholar
  30. Cruz-Hernández M, Contreras-Esquivel JC, Lara F, Rodríguez R, Aguilar CN (2005) Isolation and evaluation of tannin-degrading fungal strains from the Mexican desert. Z Naturforsch C 60:844–848CrossRefGoogle Scholar
  31. Doi S, Shinmyo A, Enatsu T, Terui G (1973) Growth associated production of tannase by a strain of Aspergillus oryzae. J Ferment Technol 61:768–774Google Scholar
  32. Elsherbiny EA, Amin BH, Baka ZA (2016) Efficiency of pomegranate (Punica granatum L.) peels extract as a high potential natural tool towards Fusarium dry rot on potato tubers. Postharvest Biol Technol 111:256–263. CrossRefGoogle Scholar
  33. El-Tanash AB, Sherief AA, Nour A (2011) Catalytic properties of immobilized tannase produced from Aspergillus aculeatus compared with free enzymes. Braz J Chem Eng 28(3):381–391. CrossRefGoogle Scholar
  34. Endo EH, Garcia Cortez DA, Ueda-Nakamura T, Nakamura CV, Dias Filho BP (2010) Potent antifungal activity of extracts and pure compound isolated from pomegranate peels and synergism with fluconazole against Candida albicans. Res Microbiol 161:534–540. CrossRefPubMedGoogle Scholar
  35. European Pharmacopoeia (2005) Fifth edition, vol 2. Council of Europe, Strasbourg, p 2534Google Scholar
  36. Evans TN, Seviour RJ (2012) Estimating biodiversity of fungi in activated sludge communities using culture-independent methods. Microb Ecol 63:773–786. CrossRefPubMedGoogle Scholar
  37. 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. CrossRefGoogle Scholar
  38. Fathi S, Hajizadeh Y, Nikaeen M, Gorbani M (2017) Assessment of microbial aerosol emissions in an urban wastewater treatment plant operated with activated sludge process. Aerobiologia 33:507–515. CrossRefGoogle Scholar
  39. Filgueira D, Moldes D, Fuentealba C, García DE (2017) Condensed tannins from pine bark: a novel wood surface modifier assisted by laccase. Ind Crop Prod 103:185–194. CrossRefGoogle Scholar
  40. Food and Agriculture Organization of the United Nations (2009) Compendium of food additive specifications, Joint FAO/WHO Expert Committee on Food Additives, 71st meeting 2009, p. 99.
  41. Ganga PS, Nandy SC, Santappa M (1977) Effect of environmental factors on the production of fungal tannase. Leather Sci 24:8–16Google Scholar
  42. Gao D, Zeng Y, Wen X, Qian Y (2008) Competition strategies for the incubation of white rot fungi under non-sterile conditions. Process Biochem 43:937–944. CrossRefGoogle Scholar
  43. Giovando S, Pizzi A, Pasch H, Pretorius N (2013) Structure and oligomers distribution of commercial Tara (Caesalpinia spinosa) hydrolysable tannin. ProLigno 9:22–31Google Scholar
  44. Gnanamani A, Sekaran G, Babu M (2001) Removal of cross-linked and open chain polymeric tannin substrates using heme peroxidases of Phanerochaete chrysosporium. Bioprocess Biosyst Eng 24:211–217. CrossRefGoogle Scholar
  45. González-García S, Feijoo G, Heathcote C, Kandelbauer A, Moreira MT (2011) Environmental assessment of green hardboard production coupled with a laccase activated system. J Clean Prod 19:445–453. CrossRefGoogle Scholar
  46. Govindarajan RK, Revathi S, Rameshkumar N, Krishnan M, Kayalvizhi M (2016) Microbial tannase: current perspectives and biotechnological advances. Biocatal Agric Biotechnol 6:168–175. CrossRefGoogle Scholar
  47. Gupta PD, Birdi TJ (2017) Development of botanicals to combat antibiotic resistance. J Ayurveda Integr Med 8:266–275. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Hadi TA, Banerjee R, Bhattacharya BC (1994) Optimization of tannase biosynthesis by a newly isolated Rhizopus oryzae. Bioprocess Eng 11:239–242. CrossRefGoogle Scholar
  49. Haslam E (1981) Vegetable tannins. In: Stumpf PK, Conn EE (eds) The biochemistry of plants. Academic Press, London, pp 527–557Google Scholar
  50. Haslam E (1996) Natural polyphenols (vegetable tannins) as drugs: possible modes of action. J Nat Prod 59:205–215. CrossRefPubMedGoogle Scholar
  51. Haslam E, Stangroom JE (1966) The esterase and depside activities of the tannase. Biochem J 99:28–31CrossRefGoogle Scholar
  52. Haslan E (1996) Natural polyphenols (vegetable tannins) as drugs. Possible model of action. J Nat Prod 59:205–215. CrossRefGoogle Scholar
  53. He Q, Yao K, Sun D, Shi B (2007) Biodegradability of tannin-containing wastewater from leather industry. Biodegradation 18:465–472. CrossRefPubMedGoogle Scholar
  54. Herrera Bravo de Laguna I, Toledo Marante FJ, Mioso R (2015) Enzymes and bioproducts produced by the ascomycete fungus Paecilomyces variotii. J Appl Microbiol 119:1455–1466. CrossRefPubMedGoogle Scholar
  55. Herrero M, Stuckey DC (2015) Bioaugmentation and its application in wastewater treatment: a review. Chemosphere 140:119–128. CrossRefPubMedGoogle Scholar
  56. Hintermeyer BH, Tavani EL (2013) Adsorption, biosorption and bioaccumulation used to remove chromium(III) from tanning wastewaters: a critical review. Soc Leather Technol Chem 97:231–237Google Scholar
  57. Hu Q, Luo C, Zhang Q, Luo Z (2013) Isolation and characterization of a Laccase gene potentially involved in proanthocyanidin polymerization in oriental persimmon (Diospyros kaki Thunb.) fruit. Mol Biol Rep 40:2809–2820. CrossRefPubMedGoogle Scholar
  58. Huang W, Li Z, Niu H, Li L, Lin W, Yang J (2007) Utilization of acorn fringe for ellagic acid production by Aspergillus oryzae and Endomyces fibuliger. Bioresour Technol 99:3552–3558. CrossRefPubMedGoogle Scholar
  59. Iibuchi S, minoda Y, Yamada K (1967) Studies on tannin acyl hydrolase of microorganisms. Part II A new method determining the enzyme activity using the change of ultra violet absorption. Agric Biol Chem 31:513–518Google Scholar
  60. Ijoma GN, Tekere M (2017) Potential microbial applications of co-cultures involving ligninolytic fungi in the bioremediation of recalcitrant xenobiotic compounds. Int J Environ Sci Technol 14:1787–1806. CrossRefGoogle Scholar
  61. Institute of Medicine (2003) Food chemicals codex: fifth edition. The National Academies Press, Washington, DC. CrossRefGoogle Scholar
  62. Iqbal HMN, Kyazze G, Tron T, Keshavarz T (2018) Laccase from Aspergillus niger: a novel tool to graft multifunctional materials of interests and their characterization. Saudi J Biol Sci 25:545–550. CrossRefPubMedGoogle Scholar
  63. Itoh N, Takagi S, Miki A, Kurokaw J (2016) Characterization and cloning of laccase gene from Hericium coralloides NBRC 7716 suitable for production of epitheaflagallin 3-O-gallate. Enzym Microb Technol 82:125–132. CrossRefGoogle Scholar
  64. Jana A, Maity C, Halder SK, Mondal KC, Pati BR, Das Mohapatra PK (2012) Tannase production by Penicillium purpurogenum PAF6 in solid state fermentation of tannin-rich plant residues following OVAT and RSM. Appl Biochem Biotechnol 167:1254–1269. CrossRefPubMedGoogle Scholar
  65. Janusz G, Pawlik A, Sulej J, Swiderska-Burek U, Jarosz-Wilkołazka A, Paszczynski A (2017) Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution. FEMS Microbiol Rev 41:941–962. CrossRefPubMedPubMedCentralGoogle Scholar
  66. Jiménez N, Curiel JA, Reverón I, de las Rivas B, Muñoz R (2013) Uncovering the Lactobacillus plantarum WCFS1 gallate decarboxylase involved in tannin degradation. Appl Environ Microbiol 79(14):4253–4263. CrossRefPubMedPubMedCentralGoogle Scholar
  67. Karpe AV, Beale DJ, Godhani NB, Morrison PD, Harding IH, Palombo EA (2015) Untargeted metabolic profiling of winery-derived biomass waste degradation by Penicillium chrysogenum. J Agric Food Chem 63:10696–10704. CrossRefPubMedGoogle Scholar
  68. Kasieczka-Burnecka M, Kuc K, Kalinowska H, Knap M, Turkiewicz M (2007) Purification and characterization of two cold-adapted extracellular tannin acyl hydrolases from an Antarctic strain Verticillium sp. P9. Appl Microbiol Biotechnol 77:77–89. CrossRefPubMedGoogle Scholar
  69. Kharchoufi S, Licciardello F, Siracusa L, Muratore G, Hamdi M, Restuccia C (2018) Antimicrobial and antioxidant features of “Gabsi” pomegranate peel extracts. J Indcrop 111:345–352. CrossRefGoogle Scholar
  70. Knudson L (1913) Tannic acid fermentation. J Biol Chem 14:159–184Google Scholar
  71. Kumar S, Beniwal V, Kumar N, Kumar A, Chhokar V, Khaket TP (2015) Biochemical characterization of immobilized tannase from Aspergillus awamori. Biocatal Agric Biotechnol 4:398–403. CrossRefGoogle Scholar
  72. 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 29:497–503CrossRefGoogle Scholar
  73. Lekha PK, Lonsane BK (1997) Production and application of tannin acyl hydrolase: state of the art. Adv Appl Microbiol 44:215–260. CrossRefPubMedGoogle Scholar
  74. Lewis JA, Starkey RL (1969) Decomposition of plant tannins by some soil microorganisms. Soil Sci 107:235–241CrossRefGoogle Scholar
  75. Leyva-Diaz J, Martin-Pascual J, Poyatos JM (2017) Moving bed biofilm reactor to treat wastewater. Int J Environ Sci Technol 14:881–910. CrossRefGoogle Scholar
  76. Li MS, Yao K, He Q, Jia DY (2006) Biodegradation of gallotannins and ellagitannins. J Basic Microbiol 46:68–84. CrossRefPubMedGoogle Scholar
  77. Liu J, Li J, Tao Y, Sellamuthu B, Walsh R (2017) Analysis of bacterial, fungal and archaeal populations from a municipal wastewater treatment plant developing an innovative aerobic granular sludge process. World J Microbiol Biotechnol 33:14. CrossRefPubMedGoogle Scholar
  78. Lofrano G, Meric S, Zengin GE, Orhon D (2013) Chemical and biological treatment technologies for leather tannery chemicals and wastewaters: a review. Sci Total Environ 461:265–281. CrossRefPubMedGoogle Scholar
  79. Ma W, Zhao F, Ye Q, Hu Z, Yan D, Hou J, Yang Y (2015) Production and partial purification of tannase from Aspergillus ficuum Gim 3.6. Prep Biochem Biotechnol 45:754–768. CrossRefPubMedGoogle Scholar
  80. 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. CrossRefGoogle Scholar
  81. 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. CrossRefGoogle Scholar
  82. Martinez AT (2002) Molecular biology and structure-function of lignin-degrading heme peroxidases. Enzym Microb Technol 30:425–444. CrossRefGoogle Scholar
  83. Mata-Gómez M, Mussatto SI, Rodríguez R, Teixeira JA, Martinez JL, Hernandez A, Aguilar CN (2009) Gallic acid production with mouldy polyurethane particles obtained from solid state culture of Aspergillus niger GH1. Appl Biochem Biotechnol 176:1131–1140. CrossRefGoogle Scholar
  84. Meier AK, Worch S, Böer E, Hartmann A, Mascher M, Marzec M, Scholz U, Riechen J, Baronian K, Schauer F, Bode R, Kunze G (2017) Agdc1p – a Gallic acid decarboxylase involved in the degradation of tannic acid in the yeast Blastobotrys (Arxula) adeninivorans. Front Microbiol 8:1777. CrossRefPubMedPubMedCentralGoogle Scholar
  85. Mishra V, Jana AK (2017) Fungal pretreatment of sweet sorghum bagasse with combined CuSO4-gallic acid supplement for improvement in lignin degradation, selectivity, and enzymatic saccharification. Appl Biochem Biotechnol 183:200–217. CrossRefPubMedGoogle Scholar
  86. Mishra V, Jana AK, Jana MM, Gupta A (2017) Synergistic effect of syringic acid and gallic acid supplements in fungal pretreatment of sweet sorghum bagasse for improved lignin degradation and enzymatic saccharification. Process Biochem 55:116–125. CrossRefGoogle Scholar
  87. Moreira F, Boaventura RAR, Brillas E, Vilar VJP (2015) Remediation of a winery wastewater combining aerobic biological oxidation and electrochemical advanced oxidation processes. Water Res 75:95–108. CrossRefPubMedGoogle Scholar
  88. Mueller-Harvey I, McAllan AB (1992) Tannins. Their biochemistry and nutritional properties. In: Morrison IM (ed) Advances in plant cell biochemistry and biotechnology. JAI Press Ltd., London, pp 151–217Google Scholar
  89. Munz G, De Angelis D, Goria R, Moric G, Casarci M, Lubello C (2009) The role of tannins in conventional and membrane treatment of tannery wastewater. J Hazard Mater 164:733–739. CrossRefPubMedGoogle Scholar
  90. Murugan K, Saravanababu S, Arunachalam M (2007) Screening of tannin acyl hydrolase (EC. producing tannery effluent fungal isolates using simple agar plate and SmF process. Bioresour Technol 98:946–949. CrossRefPubMedGoogle Scholar
  91. Mutabaruka R, Hairiah K, Cadisch G (2007) Microbial degradation of hydrolysable and condensed tannin polyphenol-protein complexes in soils from different land-use histories. Soil Biol Biochem 39:1479–1492. CrossRefGoogle Scholar
  92. Natarajan R, Manivasagan R (2018) Treatment of tannery effluent by passive uptake parametric studies and kinetic modeling. Environ Sci Pollut Res 25:5071–5075. CrossRefGoogle Scholar
  93. Niemetz R, Gross GG (2005) Enzymology of gallotannin and ellagitannin biosynthesis. Phytochemistry 66:2001–2011. CrossRefPubMedGoogle Scholar
  94. Ong C-B, Annuar MSM (2018) Immobilization of cross-linked tannase enzyme on multiwalled carbon nanotubes and its catalytic behavior. Prep Biochem Biotechnol 48(2):181–187. CrossRefPubMedGoogle Scholar
  95. Ordonez RM, Colombo I, Alberto MR, Isla MI (2011) Production of tannase from wood-degrading fungus using as substrate plant residues: purification and characterization. World J Microbiol Biotechnol 27:2325–2333. CrossRefGoogle Scholar
  96. Pane C, Fratianni F, Parisi M, Nazzaro F, Zaccardelli M (2016) Control of Alternaria post-harvest infections on cherry tomato fruits by wild pepper phenolic-rich extracts. Crop Prot 84:81–87. CrossRefGoogle Scholar
  97. Panno L, Bruno M, Voyron S, Anastasi A, Gnavi G, Miserere L, Varese GC (2013) Diversity, ecological role and potential biotechnological applications of marine fungi associated to the seagrass Posidonia oceanica. New Biotechnol 30:685–694. CrossRefGoogle Scholar
  98. Pasch H, Pizzi A (2002) Considerations on the macromolecular structure of chestnut ellagitannins by matrix-assisted laser desorption/ionization-time-of-flight mass spectrometry. J Appl Polym Sci 85:429–437. CrossRefGoogle Scholar
  99. Pasch H, Pizzi A, Rode K (2001) MALDI-TOF mass spectrometry of polyflavonoid tannins. Polymer 42:7531–7539. CrossRefGoogle Scholar
  100. Perovano N, da Silva KF, Lopez AMQ (2011) Fungic decomposition of tannic acid and other compounds from agri-industrial effluent. Acta Sci-Technol 33:145–153. CrossRefGoogle Scholar
  101. Piscitelli A, Giardina P, Lettera V, Pezzella C, Sannia G, Farmaco V (2011) Induction and transcriptional regulation of laccases in fungi. Curr Genomics 12:104–112. CrossRefPubMedPubMedCentralGoogle Scholar
  102. Pizzi A, Pasch H, Rode K, Giovando S (2009) Polymer structure of commercial hydrolyzable tannins by matrix-assisted laser desorption/ionization-time-of-flight mass spectrometry. J Appl Polym Sci 113:3847–3859. CrossRefGoogle Scholar
  103. Plodpai P, Chuenchitt S, Petcharat V, Chakthong S, Voravuthikunchai SP (2013) Anti-Rhizoctonia solani activity by Desmos chinensis extracts and its mechanism of action. Crop Prot 43:65–71. CrossRefGoogle Scholar
  104. Prashanth D, Asha MK, Amit A (2001) Antibacterial activity of Punica granatum. Fitoterapia 72:171–173. CrossRefPubMedGoogle Scholar
  105. Prigione V, Trocini B, Spina F, Poli A, Romanisio D, Giovando S, Varese GC (2018) Fungi from industrial tannins: potential application in biotransformation and bioremediation of tannery wastewaters. Appl Microbiol Biotechnol 102:4203–4216. CrossRefPubMedGoogle Scholar
  106. Purohit JS, Dutta JR, Nanda RK, Banerjee R (2006) Strain improvement for tannase production from co-culture of Aspergillus foetidus and Rhizopus oryzae. Bioresour Technol 97:795–801. CrossRefPubMedGoogle Scholar
  107. Radebe N, Rode K, Pizzi A, Giovando S, Pasch H (2013) MALDI-TOF-CID for the microstructure elucidation of polymeric hydrolysable tannins. J Appl Polym Sci 128:97–107. CrossRefGoogle Scholar
  108. Raghuwanshi S, Misra S, Kumar Saxena R (2014) Treatment of wheat straw using tannase and white-rot fungus to improve feed utilization by ruminants. J Anim Sci Biotechnol 5:13. CrossRefPubMedPubMedCentralGoogle Scholar
  109. Rajakumar GS, Nandy SC (1983) Isolation, purification, and some properties of Penicillium chrysogenum tannase. Appl Environ Microbiol 46:525–527PubMedPubMedCentralGoogle Scholar
  110. Ramos EL, Mata-Gómez MA, Rodríguez-Durán LV, Belmares RE, Rodríguez-Herrera R, Aguilar CN (2011) Catalytic and thermodynamic properties of a tannase produced by Aspergillus niger GH1 grown on polyurethane foam. Appl Biochem Biotechnol 165:1141–1151. CrossRefPubMedGoogle Scholar
  111. 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. CrossRefPubMedGoogle Scholar
  112. Rao MA, Scelza R, Acevedo F, Diez MC, Gianfreda L (2014) Enzymes as useful tools for environmental purposes. Chemosphere 107:145–162. CrossRefPubMedGoogle Scholar
  113. Ratto M, Ritschkoff A-C, Viikari L (2004) Enzymatically polymerized phenolic compounds as wood preservatives. Holzforschung 58:440–445. CrossRefGoogle Scholar
  114. Ravichandran A, Sridhar M (2017) Insights into the mechanism of lignocellulose degradation by versatile peroxidases. Curr Sci 110(1):35–42. CrossRefGoogle Scholar
  115. Rene ER, Veiga MC, Kennes C (2010) Biodegradation of gas-phase styrene using the fungus Sporothrix variecibatus: impact of pollutant load and transient operation. Chemosphere 79:221–227. CrossRefPubMedGoogle Scholar
  116. Reverón I, Jiménez N, Curiel JA, Peñas E, López de Felipe F, de las Rivas B, Muñoz R (2017) Differential gene expression by Lactobacillus plantarum WCFS1 in response to phenolic compounds reveals new genes involved in tannin degradation. Appl Environ Microbiol 83:03387–03316. CrossRefGoogle Scholar
  117. 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. CrossRefPubMedGoogle Scholar
  118. Sáez-Jiménez V, Fernández-Fueyo E, Medrano FJ, Romero A, Martínez AT, Ruiz-Dueñas FJ (2015) Improving the pH-stability of versatile peroxidase by comparative structural analysis with a naturally-stable manganese peroxidase. PLoS One 10(10):e0140984. CrossRefPubMedPubMedCentralGoogle Scholar
  119. Sahay R, Yadav RSS, Yadav KDS (2009) Purification and characterization of laccase secreted by L. lividus. Appl Biochem Biotechnol 157:311–332. CrossRefPubMedGoogle Scholar
  120. Scalbert A (1991) Antimicrobial properties of tannins. Phytochemistry 30:3875–3883CrossRefGoogle Scholar
  121. Schons PF, Rezende Lopes FC, Battestin V, Macedo GA (2011) Immobilization of Paecilomyces variotii tannase and properties of the immobilized enzyme. J Microencapsul 28(3):211–219. CrossRefPubMedGoogle Scholar
  122. Serrani Valera L, Jorge JA, Souza Guimarães LH (2015) Characterization of a multi-tolerant tannin acyl hydrolase II from Aspergillus carbonarius produced under solid-state fermentation. Electron J Biotechnol 18:464–470. CrossRefGoogle Scholar
  123. Sharma S, Bhat TK, Gupta MN (2002) Bioaffinity immobilization of tannase from Aspergillus niger on concanavalin A–Sepharose CL-4B. Biotechnol Appl Biochem 35:165–169. CrossRefPubMedGoogle Scholar
  124. Sietmann R, Uebe R, Boer E, Bode R, Kunze G, Schauer F (2010) Novel metabolic routes during the oxidation of hydroxylated aromatic acids by the yeast Arxula adeninivorans. J Appl Microbiol 108:789–799. CrossRefPubMedGoogle Scholar
  125. Silva de Lima J, Cabrera MP, de Souza Motta CM, Converti A, Carvalho LB Jr (2018) Hydrolysis of tannins by tannase immobilized onto magnetic diatomaceous earth nanoparticles coated with polyaniline. Food Res Int 107:470–476. CrossRefGoogle Scholar
  126. Silva de Lima J, Cruz R, Cordoville Fonseca J, Valente de Medeiros E, de Holanda Cavalcanti Maciel M, Aparecida Moreira K, de Souza Motta C (2014) Production, characterization of tannase from Penicillium montanense URM 6286 under SSF using agroindustrial wastes, and application in the clarification of grape juice (Vitis vinifera L.). Sci World J 2014:1–9. CrossRefGoogle Scholar
  127. Song Z, Burns RG (2005) Depolymerisation and biodegradation of a synthetic tanning agent by activated sludges, the bacteria Arthrobacter globiformis and Comamonas testosteroni, and the fungus Cunninghamella polymorpha. Biodegradation 16:305–318. CrossRefPubMedGoogle Scholar
  128. Spennati F (2018) Use of fungi and bacteria for the removal of recalcitrant compounds from tannery wastewater. PhD Thesis. Department of Civil and Environmental Engineering University of Florence and Department of Chemical, Biological and environmental engineering Autonomous University of BarcelonaGoogle Scholar
  129. Spennati F, Mora M, Guisasola A, Bardi A, Tigini V, Gabriel D, Munz G (2017) Quebracho tannin treatment with Aspergillus tubingensis MUT 990 immobilized in polyurethane foam cubes in a novel submerged cage reactor. In: Book of abstracts of 10th international conference on biofilm reactors. Dublin, Ireland, 9–12 May 2017Google Scholar
  130. Spennati F, Tigini V, Spina F, Varese GC, Bardi A, Siracusa G, Becarelli S, Di Gregorio, S, Petroni, G, Mori G, Munz, G (2016) Enhancing the tannins biodegradation with Aspergillus tubingensis and Chaetomium sp.: cosubstrates batch tests. In: SIDISA 2016, X international symposium on sanitary and environmental engineering, p. 1–9. Rome, Italy, 19–23 June 2016Google Scholar
  131. Spina F, Romagnolo A, Anastasi A, Tigini V, Prigione V, Varese GC (2012) Selection of strains and carriers to combine fungi and activated sludge in wastewater bioremediation. Environ Eng Manag J 11:1789–1796CrossRefGoogle Scholar
  132. Svobodová K, Novotný C (2018) Bioreactors based on immobilized fungi: bioremediation under non-sterile conditions. Appl Microbiol Biotechnol 102:39–46. CrossRefPubMedGoogle Scholar
  133. Tagger S, Perissol C, Gil G, Vogt G, Le Pet J (1998) Phenoloxidases of the white-rot fungus Marasmius quercophilus isolated from an evergreen oak litter (Quercus ilex L.). Enzym Microb Technol 23:372–379. CrossRefGoogle Scholar
  134. Tehranifar A, Selahvarzi Y, Kharrazi M, Bakhsh VJ (2011) High potential of agro-industrial by-products of pomegranate (Punica granatum L.) as the powerful antifungal and antioxidant substances. Ind Crop Prod 34:1523–1527. CrossRefGoogle Scholar
  135. Tigini V, Bevione F, Prigione V, Poli A, Ranieri L, Spennati F, Munz G, Varese GC (2018) Tannery mixed liquors froman ecotoxicological and mycological point of view: risks vs potential biodegradation application. Sci Tot Environ 627:835–843. CrossRefGoogle Scholar
  136. Tigini V, Varese GC (2018) Biosorption with autochthonous and allochthonous fungal biomasses for bioremediation and detoxification of landfill leachate. Environ Earth Sci 77:342. CrossRefGoogle Scholar
  137. Tomás-Cortázar J, Plaza-Vinuesa L, de las Rivas B, Lavín JJ, 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. CrossRefGoogle Scholar
  138. 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. CrossRefGoogle Scholar
  139. Vasconcelos LCS, Sampaio MCC, Sampaio FC, Higino JS (2003) Use of Punica granatum as an antifungal agent against candidosis associated with denture stomatitis. Mycoses 46:192–196CrossRefGoogle Scholar
  140. Vattem DA, Shetty K (2002) Solid-state production of phenolic antioxidants from cranberry pomace by Rhizopus oligosporus. Food Biotechnol 16:189–210. CrossRefGoogle Scholar
  141. Vattem DA, Shetty K (2003) Ellagic acid production and phenolic antioxidants activity in cranberry pomace (Vaccinium macrocarpon) mediated by Lentinus edodes using a solid-state system. Process Biochem 39:367–379. CrossRefGoogle Scholar
  142. Venter PB, Sisa M, Van der Merwe MJ, Bonnet SL, Van der Westhuizen JH (2012) Analysis of commercial proanthocyanidins. Part 1: the chemical composition of quebracho (Schinopsis lorentzii and Schinopsis balansae) heartwood extract. Phytochemistry 73:95–105. CrossRefPubMedGoogle Scholar
  143. Vepsalainen M, Kivisaari H, Pulliainen M, Oikari A, Sillanpaa M (2011) Removal of toxic pollutants from pulp mill effluents by electrocoagulation. Sep Purif Technol 81:141–150. CrossRefGoogle Scholar
  144. Voravuthikunchai SP, Sririrak T, Limsuwan S, Supawita T, Iida T, Honda T (2005) Inhibitory effects of active compounds from Punica granatum pericarp on verocytotoxin production by enterohemorrhagic Escherichia coli O157:H7. J Health Sci 51:590–596. CrossRefGoogle Scholar
  145. Widsten P, Hummer A, Heathcote C, Kandelbauer A (2009) A preliminary study of green production of fiberboard bonded with tannin and laccase in a wet process. Holzforschung 63:545–550. CrossRefGoogle Scholar
  146. Wu CZ, Zhang F, Li LJ, Jiang ZD, Ni H, Xiao AX (2018) Novel optimization strategy for tannase production through a modified solid-state fermentation system. Biotechnol Biofuels 11:92. CrossRefPubMedPubMedCentralGoogle Scholar
  147. Yague S, Terron MC, Gonzalez T, Zapico E, Bocchini P, Galletti GC, Gonzalez AE (2000) Biotreatment of tannin-rich beer-factory wastewater with white-rot basidiomycete Coriolopsis gallica monitored by pyrolysis/gas chromatography/mass spectrometry. Rapid Commun Mass Spectrom 14:905–910.<905::AID-RCM963>3.0.CO;2-7 CrossRefPubMedGoogle Scholar
  148. Yamada H, Adachi C, Watanabe M, Sato N (1968) Studies of fungal tannase. Part I. formation, purification and catalytic properties of tannase of Aspergillus flavus. Agric Biol Chem 32:1070–1078Google Scholar
  149. Yamaguchi H, Maeda Y, Sakata I (1998) Applications of phenol dehydrogenative polymerization by laccase to bonding among woody-fibers. Mokuzai Gakkaishi 38:931–937Google Scholar
  150. Yao J, Guo GS, Ren GH, Liu YH (2014) Production, characterization and applications of tannase. J Mol Catal B Enzym 101:137–147. CrossRefGoogle Scholar
  151. Yu X, Li Y, Wang C, Wu D (2004) Immobilization of Aspergillus niger tannase by microencapsulation and its kinetic characteristics. Biotechnol Appl Biochem 40:151–155. CrossRefPubMedGoogle Scholar
  152. Zakipour-Molkabadi E, Hamidi-Esfahani Z, Sahari MA, Azizi MH (2013) A new native source of tannase producer, Penicillium sp. EZ-ZH190: characterization of the enzyme. Iran J Biotechnol 11(4):244–250. CrossRefGoogle Scholar
  153. Zeida M, Weiser M, Yoshida T, Sugio T, Nagasawa T (1998) Purification and characterization of gallic acid decarboxylase from Pantoea agglomerans T71. Appl Environ Microbiol 64(12):4743–4747PubMedPubMedCentralGoogle Scholar
  154. Zerva A, Manos N, Vouyiouka S, Christakopoulos P, Topakas E (2016) Bioconversion of biomass-derived phenols catalyzed by Myceliophthora thermophila laccase. Molecules 21:550. CrossRefGoogle Scholar
  155. 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. CrossRefPubMedGoogle Scholar
  156. Zheng ZX, Shetty K (2000) Solid-state bioconversion of phenolics from cranberry pomace and role of Lentinus edodes beta-glucosidase. J Agric Food Chem 48:895–900. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Life Sciences and Systems BiologyUniversity of TurinTurinItaly
  2. 2.Centro Ricerche per la Chimica Fine Srl for Silvateam SpaSan Michele MondovìItaly

Personalised recommendations