Abstract
Tannins are a complex family of polyphenolic compounds, widely distributed in the plant kingdom where they act as growth inhibitors towards many microorganisms including bacteria, yeasts, and fungi. Tannins are one of the major components of tannery wastewaters and may cause serious environmental pollution. In the present study, four different tannins (the hydrolysable chestnut ellagitannin and tara gallotannin and the condensed quebracho and wattle tannins) were characterized from a mycological point of view with the aim of selecting fungal strains capable of growing in the presence of high tannin concentration and thus potentially useful in industrial biotransformations of these compounds or in the bioremediation of tannery wastewaters. A total of 125 isolates of filamentous fungi belonging to 10 species and four genera (Aspergillus, Paecilomyces, Penicillium, and Talaromyces) were isolated from the tannin industrial preparations. Miniaturized biotransformation tests were set up with 10 fungal strains and the high-performance liquid chromatography (HPLC) analysis pointed out a strong activity of all the tested fungi on both chestnut and tara tannins. Two strains (Aspergillus tubingensis MUT 990 and Paecilomyces variotii MUT 1125), tested against a real tannery wastewater, were particularly efficient in chemical oxygen demand (COD) and tannin removal (> 60%), with a detoxification above 74%. These results indicate that these fungi are potentially exploitable in the treatment of tannery wastewaters.
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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. https://doi.org/10.1007/s00253-007-1000-2
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. https://doi.org/10.1007/s00253-007-1276-2
Anastasi A, Spina F, Prigione V, Tigini V, Giansanti P, Varese GC (2010) Scale-up of a bioprocess for textile wastewater treatment using Bjerkandera adusta. Bioresour Technol 101:3067–3075. https://doi.org/10.1016/j.biortech.2009.12.067
Ascacio-Valdes JA, Buenrostro JJ, De la Cruz R, Sepulveda L, Aguilera AF, Prado A, Contreras JC, Rodriguez R, Aguilar CN (2016) Fungal biodegradation of pomegranate ellagitannins. J Basic Microbiol 54:28–34. https://doi.org/10.1002/jobm.201200278
Bardei F, Bouziane H, Trigo MD, Ajouray N, El Haskouri F, Kadiri M (2017) Atmospheric concentrations and intradiurnal pattern of Alternaria and Cladosporium conidia in Tétouan (NW of Morocco). Aerobiologia 33:221–228. https://doi.org/10.1007/s10453-016-9465-z
Bhat TK, Singh B, Sharma OP (1998) Microbial degradation of tannins—a current perspective. Biodegradation 9:343–357. https://doi.org/10.1023/A:1008397506963
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. https://doi.org/10.1016/j.fbp.2014.10.007
Cassano A, Adzet J, Molinari R, Buonomenna MG, Roig J (2003) Membrane treatment by nanofiltration of exhausted vegetable tannin liquors from the leather industry. Water Res 37:2426–2434. https://doi.org/10.1016/S0043-1354(03)00016-2
Chambergo FS, Valencia EY (2016) Fungal biodiversity to biotechnology. Appl Microbiol Biotechnol 100:2567–2577. https://doi.org/10.1007/s00253-016-7305-2
Chowdhury SA, Vijayaraghavan R, MacFarlane DR (2010) Distillable ionic liquid extraction of tannins from plant materials. Green Chem 12:1023–1028. https://doi.org/10.1039/b923248f
Clarke KR, Warwick RM (2014) Change in marine communities: an approach to statistical analysis and interpretation. PRIMER-E Ltd, Plymouth
Cruz-Hernandez M, Augur C, Rodriguez R, Contreras-Esquivel JC, Aguilar CN (2006) Evaluation of culture conditions for tannase production by Aspergillus niger GH1. Food Technol Biotechnol 44:541–544
de Souza JM, Montalvao MF, da Silva AR, Rodrigues ASD, Malafaia G (2017) A pioneering study on cytotoxicity in Australian parakeets (Melopsittacus undulates) exposed to tannery effluent. Chemosphere 175:521–533. https://doi.org/10.1016/j.chemosphere.2017.02.087
Demirel R, Sen B, Kadaifciler D, Yoltas A, Okten S, Okzale E, Berikten D, Samson RA, Uztan AH, Yilmaz N (2017) Indoor airborne fungal pollution in newborn units in Turkey. Environ Monit Assess 189:362. https://doi.org/10.1007/s10661-017-6051-y
Deschamps A, Otuk G, Lebeault J (1983) Production of tannase and degradation chestnut tannin by bacteria. J Ferment Technol 61:55–59
Domsch KH, Gams W, Anderson TH (1980) Compendium of soil fungi. Academic Press, London
Edelmann A, Lendi B (2002) Toward the optical tongue: flow-through sensing of tannin-protein interactions based on FTIR spectroscopy. J Am Chem Soc 124:14741–14747. https://doi.org/10.1021/ja026309v
European Commission (2010) Directive 2010/75/EU of the European Parliament and of the Council on Industrial Emissions (integrated pollution prevention and control). Off J Eur Union L334/17
Giovando S, Pizzi A, Pasch H, Pretorius N (2013) Structure and oligomers distribution of commercial tara (Caesalpinia spinosa) hydrolysable tannin. ProLigno 9:22–31
Gnavi G, Garzoli L, Poli A, Prigione V, Burgaud G, Varese GC (2017) The culturable mycobiota of Flabellia petiolata: first survey of marine fungi associated to a Mediterranean green alga. PLoS One 12:e0175941. https://doi.org/10.1371/journal.pone.0175941
Govindarajan RK, Revathi S, Rameshkumar N, Krishnan M, Kayalvizhi N (2016) Microbial tannase: current perspectives and biotechnological advances. Biocatal Agric Biotechnol 6:168–175. https://doi.org/10.1016/j.bcab.2016.03.011
Hasegawa MC, Barbosa AM, Takashima K (2011) Biotreatment of industrial tannery wastewater using Botryosphaeria rhodina. J Serb Chem Soc 76:439–446. https://doi.org/10.2298/JSC100603039H
International Organization for Standardization (2004) ISO 8692:2004 water quality—freshwater algal growth inhibition test with unicellular green algae. International Organization for Standardization, Geneva
International Organization for Standardization (2012) ISO 14088:2012 leather—chemical tests—quantitative analysis of tanning agents by filter method. International Organization for Standardization, Geneva
Kanth SV, Venba R, Madhan B, Chandrababu NK, Sadulla S (2009) Cleaner tanning practices for tannery pollution abatement: role of enzymes in eco-friendly vegetable tanning. J Clean Prod 17:507–515. https://doi.org/10.1016/j.jclepro.2008.08.021
Kiffer E, Morelet M (1997) Les Deuteromycetes: classification et cles d'Identification Generique. INRA Editions, Paris
Knudson L (1913) Tannic acid fermentation. J Biol Chem 14:159–184
Lara-Victoriano F, Veana F, Hernandez-Castillo FD, Aguilar CN, Reyes-Valdes MH, Rodriduez-Herrera R (2017) Variability among strains of Aspergillus section Nigri with capacity to degrade tannic acid isolated from extreme environments. Arch Microbiol 199:77–84. https://doi.org/10.1007/s00203-016-1277-6
Lekha PK, Lonsane BK (1997) Production and application of tannin acyl hydrolase: state of the art. Adv Appl Microbiol 44:215–260. https://doi.org/10.1016/S0065-2164(08)70463-5
Lewis JA, Starkey RL (1969) Decomposition of plant tannins by some soil microorganisms. Soil Sci 107:235–241
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. https://doi.org/10.1080/10826068.2014.952384
Messini A, Buccioni A, Minieri S, Mannelli F, Mugnai L, Comparini C, Venturi M, Viti C, Pezzati A, Rapaccini S (2017) Effect of chestnut tannin extract (Castanea sativa Miller) on the proliferation of Cladosporium cladosporioides on sheep cheese rind during the ripening. Int Dairy J 66:6–12. https://doi.org/10.1016/j.idairyj.2016.10.012
Munz G, De Angelis D, Gori R, Mori G, Casarci M, Lubello C (2009) The role of tannins in conventional and membrane treatment of tannery wastewater. J Hazard Mater 164:733–739. https://doi.org/10.1016/j.jhazmat.2008.08.070
Okoduwa SIR, Igiri B, Udeh CB, Edenta C, Gauje B (2017) Tannery effluent treatment by yeast species isolates from watermelon. Toxics 5:1–10. https://doi.org/10.3390/toxics5010006
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. https://doi.org/10.1002/app.10618
Pasch H, Pizzi A, Rode K (2001) MALDI-TOF mass spectrometry of polyflavonoid tannins. Polymer 42:7531–7539. https://doi.org/10.1016/S0032-3861(01)00216-6
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. https://doi.org/10.1002/app.30377
Poli A, Lazzari A, Prigione V, Voyron S, Spadaro D, Varese GC (2016) Influence of plant genotype on the cultivable fungi associated to tomato rhizosphere and roots in different soils. Fungal Biol 120:862–872. https://doi.org/10.1016/j.funbio.2016.03.008
Prigione V, Zerlottin M, Refosco D, Tigini V, Anastasi A, Varese GC (2009) Chromium removal from a real tanning effluent by autochthonous and allochthonous fungi. Bioresour Technol 100:2770–2776. https://doi.org/10.1016/j.biortech.2009.01.002
Radebe N, Rode K, Pizzi A, Giovando S, Pasch H (2013a) MALDI-TOF-CID for the microstructure elucidation of polymeric hydrolysable tannins. J Appl PolymSci 128:97–107. https://doi.org/10.1002/app.38156
Radebe N, Rode K, Pizzi A, Pasch H (2013b) Microstructure elucidation of polyflavonoid tannins by MALDI-TOF-CID. J Appl Polym Sci 127:1937–1950. https://doi.org/10.1002/app.37568
Romero-Dondiz EM, Almazan JE, Rajal VB, Castro-Vidaurre EF (2015) Removal of vegetable tannins to recover water in the leather industry by ultrafiltration polymeric membranes. Chem Eng Res Des 93:727–735. https://doi.org/10.1016/j.cherd.2014.06.022
Samson RA, Houbraken J, Thrane U, Frisvad JC, Andersen B (2010) Food and indoor fungi. CBS-KNAW Fungal Biodiversity Centre, Utrecht
Sathvika T, Manasi M, Rajesh V, Rajesh N (2015) Prospective application of Aspergillus species immobilized in sodium montmorillonite to remove toxic hexavalent chromium from wastewater. RSC Adv 5:107031–107044. https://doi.org/10.1039/c5ra22778j
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. https://doi.org/10.1155/2014/182025
Silva O, Duarte A, Pimentel M, Viegas S, Barroso H, Machado J, Pires I, Cabrita J, Gomes E (1997) Antimicrobial activity of Terminalia macroptera root. J Ethnopharmacol 57:203–207. https://doi.org/10.1016/S0378-8741(97)00068-8
Tigini V, Prigione V, Varese GC (2014) Mycological and ecotoxicological characterisation of landfill leachate before and after traditional treatments. Sci Total Environ 487:335–341. https://doi.org/10.1016/j.scitotenv.2014.04.026
van Diepeningen AD, Debets AJM, Varga J, van der Gaag M, Swart K, Hoekstra RF (2004) Efficient degradation of tannic acid by black Aspergillus species. Mycol Res 108:919–925. https://doi.org/10.1017/S0953756204000747
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. https://doi.org/10.1016/j.phytochem.2011.10.006
von Arx JA (1981) The genera of fungi sporulating in pure culture. J Cramer, Vaduz
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This work was supported by Ministero dell’Istruzione, dell’Università e della Ricerca (MIUR) with the FIRB project RBFR13V3CH_002 with the title “In situ bioaugmentation to exploit the combination of fungi and bacteria for recalcitrant compounds removal.”
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Prigione, V., Trocini, B., Spina, F. et al. Fungi from industrial tannins: potential application in biotransformation and bioremediation of tannery wastewaters. Appl Microbiol Biotechnol 102, 4203–4216 (2018). https://doi.org/10.1007/s00253-018-8876-x
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DOI: https://doi.org/10.1007/s00253-018-8876-x