Abstract
Tannase catalyzes the de-esterification of tannins into gallic acid and glucose. This enzyme has extensive value in removing tannins from tea, beer, and wine. For its benefit, innovative tannase-producing organisms continue to be reported in the literature. In this study, a novel tannase-producing fungal strain with a high tolerance to tannin was isolated from corn cobs and identified as Penicillium commune HS2. Four variables, i.e., initial pH, temperature, potato peel, and tannin concentrations, were evaluated to optimize their effects on tannase production. Using central composite design (CCD) of response surface methodology (RSM) for the optimization of tannase production on potato peels, a 4.62-fold upsurge was successfully achieved. The maximum productivity of 288.48 U from 1 g of dry potato peels was obtained under solid-state fermentation (SSF) at pH 5.0, 25.1 °C, in a medium containing 1.13% and 9.99% of potato peel and tannin, respectively. The purified enzyme had a molecular weight (Mw) of 35 kDa and showed maximal activity at 40–50 °C and a pH range of 4–5, as well as a half-life of 70 min at 40 °C. Using the tannic acid as a substrate, the enzyme had a Km value of 0.217 mM and Vmax of 8.08 U/ml/min. The purified enzyme successfully reduced 33.89% of total tannin content in lemon tea after 2 h at 45 °C. It can be concluded that Penicillium commune is a potentially high-tolerant tannin fungus that may be produced commercially on potato peel waste at a low cost and has promising applications in the food sector.
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12 February 2022
A Correction to this paper has been published: https://doi.org/10.1007/s13399-022-02451-y
References
Saeed S, Aslam S, Mehmood T et al (2021) Production of gallic acid under solid-state fermentation by utilizing waste from food processing industries. Waste Biomass Valorization 12:155–163. https://doi.org/10.1007/s12649-020-00980-z
Pan J, Wang NN, Yin XJ et al (2020) Characterization of a robust and pH-stable tannase from mangrove-derived yeast Rhodosporidium diobovatum Q95. Mar Drugs 18:546. https://doi.org/10.3390/md18110546
Kumar M, Rana S, Beniwal V, Salar RK (2015) Optimization of tannase production by a novel Klebsiella pneumoniae KP715242 using central composite design. Biotechnol Rep 7:128–134. https://doi.org/10.1016/j.btre.2015.06.002
de Lima JS, Cabrera MP, de Souza Motta CM et al (2018) Hydrolysis of tannins by tannase immobilized onto magnetic diatomaceous earth nanoparticles coated with polyaniline. Food Res Int 107:470–476. https://doi.org/10.1016/j.foodres.2018.02.066
Kumar M, Singh A, Beniwal V, Salar RK (2016) Improved production of tannase by Klebsiella pneumoniae using Indian gooseberry leaves under submerged fermentation using Taguchi approach. AMB Express 6:46. https://doi.org/10.1186/s13568-016-0217-9
Chaitanyakumar A, Anbalagan M (2016) Expression, purification and immobilization of tannase from Staphylococcus lugdunensis MTCC 3614. AMB Express 6:89. https://doi.org/10.1186/s13568-016-0261-5
Kanpiengjai A, Unban K, Nguyen T-H et al (2019) Expression and biochemical characterization of a new alkaline tannase from Lactobacillus pentosus. Protein Expr Purif 157:36–41. https://doi.org/10.1016/j.pep.2019.01.005
Food and Agriculture Organization (FAO) (2019). https://www.fao.org/statistics/en/
Fritsch C, Staebler A, Happel A et al (2017) Processing, valorization and application of bio-waste derived compounds from potato, tomato, olive and cereals: a review. Sustainability 9:1492. https://doi.org/10.3390/su9081492
Galhano dos Santos R, Ventura P, Bordado JC, Mateus MM (2016) Valorizing potato peel waste: an overview of the latest publications. Rev Env Sci Biotechnol 15:585–592. https://doi.org/10.1007/s11157-016-9409-7
Venturi F, Bartolini S, Sanmartin C et al (2019) Potato peels as a source of novel green extracts suitable as antioxidant additives for fresh-cut fruits. Appl Sci 9:2431. https://doi.org/10.3390/app9122431
Singh B, Singh J, Singh JP et al (2020) Phenolic compounds in potato (Solanum tuberosum L.) peel and their health-promoting activities. Int J Food Sci Technol 55:2273–2281
Mushtaq Q, Irfan M, Tabssum F, Iqbal Qazi J (2017) Potato peels: a potential food waste for amylase production. J Food Proc Eng 40:12512. https://doi.org/10.1111/jfpe.12512
Tuysuz E, Gonul-Baltaci N, Omeroglu MA et al (2020) Co-production of amylase and protease by locally isolated thermophilic bacterium Anoxybacillus rupiensis T2 in sterile and non-sterile media using waste potato peels as substrate. Waste Biomass Valorization 11:6793–6802. https://doi.org/10.1007/s12649-020-00936-3
Kumar A, Singh A, Bilal M, Chandra R (2021) Sustainable production of thermostable laccase from agro-residues waste by Bacillus aquimaris AKRC02. In press, Cat Lett. https://doi.org/10.1007/s10562-021-03753-y
Wu C, Zhang F, Li L et al (2018) Novel optimization strategy for tannase production through a modified solid-state fermentation system. Biotechnol Biofuels 11:92. https://doi.org/10.1186/s13068-018-1093-0
Kanpiengjai A, Khanongnuch C, Lumyong S et al (2020) Co-production of gallic acid and a novel cell-associated tannase by a pigment-producing yeast Sporidiobolus ruineniae A45.2. Microb Cell Fact 19:95. https://doi.org/10.1186/s12934-020-01353-w
Sharma S, Bhat TK, Dawra RK (2000) A spectrophotometric method for assay of tannase using Rhodanine. Anal Biochem 279:85–89. https://doi.org/10.1006/abio.1999.4405
Liu TPSL, Brandão Costa RMP, de Vasconcelos Freitas DJ et al (2017) Tannase from Aspergillus melleus improves the antioxidant activity of green tea: purification and biochemical characterisation. Int J Food Sci Technol 52:652–661. https://doi.org/10.1111/ijfs.13318
Mansor A, Ramli MS, Abdul Rashid NY et al (2019) Evaluation of selected agri-industrial residues as potential substrates for enhanced tannase production via solid-state fermentation. Biocatal Agric Biotechnol 20:101216. https://doi.org/10.1016/j.bcab.2019.101216
Kumar M, Mugunthan M (2018) Evaluation of three DNA extraction methods from fungal cultures. Med J Armed Forces India 74:333–336. https://doi.org/10.1016/j.mjafi.2017.07.009
Oduro-Mensah D, Ocloo A, Lowor ST et al (2018) Isolation and characterisation of theobromine-degrading filamentous fungi. Microbiol Res 206:16–24. https://doi.org/10.1016/j.micres.2017.09.006
Gafar AA, Khayat ME, Ahmad SA et al (2020) Response surface methodology for the optimization of keratinase production in culture medium containing feathers by Bacillus sp UPM-AAG1. Catalysts 10:848. https://doi.org/10.3390/catal10080848
Xiao A, Huang Y, Ni H et al (2015) Statistical optimization for tannase production by Aspergillus tubingensis in solid-state fermentation using tea stalks. Electron J Biotechnol 18:143–147. https://doi.org/10.1016/j.ejbt.2015.02.001
Aharwar A, Parihar DK (2021) Talaromyces verruculosus tannase immobilization, characterization, and application in tea infusion treatment. Biomass Conv Bioref 1:12. https://doi.org/10.1007/s13399-020-01162-6
Al-Mraai STY, Al-Fekaiki DF, Al-Manhel AJA (2019) Purification and characterization of tannase from the local isolate of Aspergillus niger. J Appl Biol Biotechnol 7:29–34. https://doi.org/10.7324/JABB.2019.70106
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Hu G, Heitmann JA, Rojas OJ et al (2010) Monitoring cellulase protein adsorption and recovery using SDS-PAGE. Ind Eng Chem Res 49:8333–8338. https://doi.org/10.1021/ie100731b
Shao Y, Zhang Y-H, Zhang F et al (2020) Thermostable tannase from Aspergillus niger and its application in the enzymatic extraction of green tea. Molecules 25:952. https://doi.org/10.3390/molecules25040952
de Lima JS, Cabrera MP, Casazza AA et al (2018) Immobilization of Aspergillus ficuum tannase in calcium alginate beads and its application in the treatment of boldo (Peumus boldus) tea. Int J Biol Macromol 118:1989–1994. https://doi.org/10.1016/j.ijbiomac.2018.07.084
Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42. https://doi.org/10.2307/3001478
Lekha PK, Lonsane BK (1997) Production and application of tannin acyl hydrolase: state of the art. In Advances in Applied Microbiology 44:215–260. https://doi.org/10.1016/S0065-2164(08)70463-5
Lekshmi R, Arif Nisha S, Kaleeswaran B, Alfarhan AH (2020) Pomegranate peel is a low-cost substrate for the production of tannase by Bacillus velezensis TA3 under solid state fermentation. J King Saud Univ Sci 32:1831–1837. https://doi.org/10.1016/j.jksus.2020.01.022
Thiyonila B, Kannan M, Paulin Reneeta N et al (2020) Influence of tannase from Serratia marcescens strain IMBL5 on enhancing antioxidant properties of green tea. Biocatal Agric Biotechnol 27:101675. https://doi.org/10.1016/j.bcab.2020.101675
Selvaraj S, Natarajan K, Nowak A, Murty VR (2021) Mathematical modeling and simulation of newly isolated bacillus cereus M1GT for tannase production through semi-solid state fermentation with agriculture residue triphala. South Afric J Chem Eng 35:89–97. https://doi.org/10.1016/j.sajce.2020.10.001
Lima JS de, Cruz R, Fonseca JC, et al (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 182025. https://doi.org/10.1155/2014/182025
Saeed S, Bibi I, Mehmood T et al (2020) Valorization of locally available waste plant leaves for production of tannase and gallic acid by solid-state fermentation. In press, Biomass Conv Bioref. https://doi.org/10.1007/s13399-020-00989-3
Lei J, Zhang Y, Ni X et al (2021) Degradation of epigallocatechin and epicatechin gallates by a novel tannase TanHcw from Herbaspirillum camelliae. Microb Cell Fact 20:197. https://doi.org/10.1186/s12934-021-01685-1
Andrade PML, Baptista L, Bezerra CO et al (2021) Immobilization and characterization of tannase from Penicillium rolfsii CCMB 714 and its efficiency in apple juice clarification. J Food Measurement Characterization 15:1005–1013. https://doi.org/10.1007/s11694-020-00705-9
Mahmoud AE, Fathy SA, Rashad MM et al (2018) Purification and characterization of a novel tannase produced by Kluyveromyces marxianus using olive pomace as solid support, and its promising role in gallic acid production. Int J Biol Macromol 107:2342–2350. https://doi.org/10.1016/j.ijbiomac.2017.10.117
Govindarajan RK, Krishnamurthy M, Neelamegam R et al (2019) Purification, structural characterization and biotechnological potential of tannase enzyme produced by Enterobacter cloacae strain 41. Process Biochem 77:37–47. https://doi.org/10.1016/j.procbio.2018.10.013
Koseki T, Ichikawa K, Sasaki K, Shiono Y (2018) Characterization of a novel Aspergillus oryzae tannase expressed in Pichia pastoris. J Biosci Bioeng 126:553–558. https://doi.org/10.1016/j.jbiosc.2018.05.010
Tomás-Cortázar J, Plaza-Vinuesa L, de las Rivas B et al (2018) Identification of a highly active tannase enzyme from the oral pathogen Fusobacterium nucleatum subsp polymorphum. Microb Cell Fact 17:33. https://doi.org/10.1186/s12934-018-0880-4
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. https://doi.org/10.1016/j.ijbiomac.2016.06.098
Gorgulu TY, Ozdemir OD, Kipcak AS et al (2016) The effect of lemon on the essential element concentrations of herbal and fruit teas. Appl Biol Chem 59:425–431. https://doi.org/10.1007/s13765-016-0161-z
Li J, Xiao Q, Huang Y et al (2017) Tannase application in secondary enzymatic processing of inferior Tieguanyin oolong tea. Elect J Biotechnol 28:87–94. https://doi.org/10.1016/j.ejbt.2017.05.010
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Mostafa, H.S. Potato peels for tannase production from Penicillium commune HS2, a high tannin-tolerant strain, and its optimization using response surface methodology. Biomass Conv. Bioref. 13, 16765–16778 (2023). https://doi.org/10.1007/s13399-021-02205-2
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DOI: https://doi.org/10.1007/s13399-021-02205-2