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Differential Properties of Aspergillus niger Tannase Produced Under Solid-State and Submerged Fermentations

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Abstract

Significant differences on structure, stability, and catalytic properties of tannase were found when this enzyme was produced under solid-state and submerged fermentations (SSF and SmF) by Aspergillus niger. The specific activity was 5.5 times higher on SSF than in SmF. Significant differences in isoelectric points of tannases were found. The pH optima for both types of enzyme was found at 6 and the pH stability of SSF and SmF tannase were at 6 and 5–8, respectively. The optimal temperature range was from 50 to 60 °C for SmF tannase and 60 °C for SSF tannase, and both enzyme types showed tolerance to high temperatures (60–70 °C). The SSF tannase showed a major specificity for methyl gallate substrate while SmF tannase for tannic acid. All metal ions tested, had an activity inhibition from 30–46% on SSF tannase. SDS-PAGE analysis as well as gel localization studies of both SSF and SmF purified tannases showed a single band with a molecular weight of 102 and 105 kDa, respectively. Different levels of glycosylation were found among SSF and SmF purified tannases. This is the first report about structural differences among tannase produced under SSF and SmF and this study provides basis for explanation of the stability and catalytic differences observed previously for this two tannase types.

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References

  1. Adachi, O., Watanabe, M., & Yamada, H. (1968). Studies on fungal tannase. Part II. Physicochemical properties of tannase of Aspergillus flavus. J Agric Food Chem, 32, 1079–1085.

    CAS  Google Scholar 

  2. Aguilar, C. N., 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.

    Article  CAS  Google Scholar 

  3. Aguilar, C. N., Augur, C., Favela-Torres, E., & Viniegra-González, G. (2001). Induction and repression patterns of fungal tannase in solid-state and submerged cultures. Process Biochem, 36, 565–570.

    Article  CAS  Google Scholar 

  4. Aguilar, C. N., & Gutiérrez-Sánchez, G. (2001). Review: Sources, properties, applications and potential uses of tannin acyl hydrolase. Food Sci Technol Int, 7, 373–382.

    CAS  Google Scholar 

  5. Aguilar, C. N., Gutiérrez-Sánchez, G., Prado-Barragán, L. A., Rodríguez-Herrera, R., Martínez-Hernandez, J. L., & Contreras-Esquivel, J. C. (2010). Perspectives of solid state fermentation for production of food enzymes. Am J Biochem Biotechnol, 4, 354–366.

    Google Scholar 

  6. Aguilar, C. N., Rodríguez, R., Gutiérrez-Sánchez, G., Augur, C., Favela-Torres, E., Prado-Barragan, L. A., et al. (2007). Microbial tannases: Advances and perspectives. Appl Microbiol Biotechnol, 76, 47–59.

    Article  CAS  Google Scholar 

  7. Albertse EH (2002) Cloning, expression and characterization of tannase from Aspergillus species. Ms Thesis, University of the Free State, Bloemfontein, South Africa

  8. Aoki, K., Shinke, R., & Nishira, H. (1976). Chemical composition and molecular weight of yeast tannase. Agric Biol Chem, 40, 297–302.

    Article  CAS  Google Scholar 

  9. Ayed, L., & Hamdi, M. (2002). Culture conditions of tannase production by Lactobacillus plantarum. Biotechnol Lett, 24, 1763–1765.

    Article  CAS  Google Scholar 

  10. Barthomeuf, C., Regerat, F., & Pourrat, H. (1994). Production, purification and characterization of a tannase from Aspergillus niger LCF 8. J Ferment Bioeng, 77, 320–323.

    Article  CAS  Google Scholar 

  11. Beena, P. S., Soorej, M. B., Elyas, K. K., Bhat Sarita, G., & Chandrasekaran, M. (2010). Acidophilic tannase from marine Aspergillus awamori BTMFW032. J Microbiol Biotechnol, 20, 1403–1414.

    CAS  Google Scholar 

  12. Belur, P. D., Gopal, M., Nirmala, K. R., & Basavaraj, N. (2010). Production of novel cell-associated tannase from newly isolated Serratia ficaria DTC. J Microbiol Biotechnol, 20, 732–736.

    CAS  Google Scholar 

  13. Benoit, I., Asther, M., Sulzenbacher, G., Record, E., Marmuse, L., Parsiegla, G., et al. (2006). Respective importance of protein folding and glycosylation in the thermal stability of recombinant feruloyl esterase A. FEBS Lett, 580, 5815–5821.

    Article  CAS  Google Scholar 

  14. Beverini, M., & Metche, M. (1990). Identification, purification, physiochemical properties of tannase from Aspergillus oryzae. Sci Aliments, 10, 807–816.

    CAS  Google Scholar 

  15. Bhardwaj, R., Singh, B., & Bhat, T. K. (2003). Purification and characterization of tannin acyl hydrolase from Aspergillus niger MTCC 2425. J Basic Microbiol, 43, 449–461.

    Article  CAS  Google Scholar 

  16. Bhat, T. K., Singh, B., & Sharma, O. P. (1998). Microbial degradation of tannins—A current perspective. Biodegradation, 9, 343–357.

    Article  CAS  Google Scholar 

  17. Blum, H., Beier, H., & Gross, H. J. (1987). Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis, 8, 93–99.

    Article  CAS  Google Scholar 

  18. 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.

    Article  Google Scholar 

  19. Bradoo, S., Gupta, R., & Saxena, R. K. (1997). Parametric optimization and biochemical regulation of extracellular tannase from Aspergillus japonicus. Process Biochem, 32, 135–139.

    Article  CAS  Google Scholar 

  20. Costa, A. M., Ribeiro, W. X., Kato, E., Monteiro, A. R. G., & Peralta, R. M. (2008). Production of tannase by Aspergillus tamarii in submerged cultures. Braz Arch Biol Technol, 51, 399–404.

    Article  CAS  Google Scholar 

  21. Curiel, J. A., Rodríguez, H., Acebrón, I., Mancheño, J. M., De Blanca Rivas, L., & Muñoz, R. (2009). Production and physicochemical properties of recombinant Lactobacillus plantarum tannase. J Agric Food Chem, 57, 6224–6230.

    Article  CAS  Google Scholar 

  22. Das Mohapatra, P. K., Maity, C., Rao, R. S., Pati, B. R., & Mondal, K. C. (2009). Tannase production by Bacillus licheniformis KBR6: Optimization of submerged culture conditions by Taguchi DOE methodology. Food Res Int, 42, 430–435.

    Article  CAS  Google Scholar 

  23. Enemuor, S. C., & Odibo, F. J. C. (2009). Culture conditions for the production of a tannase of Aspergillus tamarii IMI388810. Afr J Biotechnol, 8, 2554–2557.

    CAS  Google Scholar 

  24. Hata, Y., Ishida, H., Ichikawa, E., Kawato, A., Suginami, K., & Imayasu, S. (1998). Nucleotide sequence of an alternative glucoamylase-encoding gene (glaB) expressed in solid-state culture of Aspergillus oryzae. Gene, 207, 127–134.

    Article  CAS  Google Scholar 

  25. 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.

    Article  CAS  Google Scholar 

  26. Iwashita, K. (2002). Recent studies of protein secretion by filamentous fungi. J Biosci Bioeng, 94, 530–535.

    CAS  Google Scholar 

  27. 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.

    Article  CAS  Google Scholar 

  28. Kumar, R. A., Gunasekaran, P., & Lakshmanan, M. (1999). Biodegradation of tannic acid by Citrobacter freundii isolated from a tannery effluent. J Basic Microbiol, 39, 161–168.

    Article  CAS  Google Scholar 

  29. Lekha, P. K., & Lonsane, B. K. (1994). Comparative titres, location and properties of tannin acyl hydrolase produced by Aspergillus niger PKL 104 in solid-state, liquid surface an submerged fermentations. Process Biochem, 29, 497–503.

    Article  CAS  Google Scholar 

  30. Lekha, P. K., & Lonsane, B. K. (1997). In S. Neidleman & A. Laskin (Eds.), Advances in Applied Microbiology vol. 44 (pp. 215–260). San Diego: Academic.

    Chapter  Google Scholar 

  31. Mahapatra, K., Nanda, R. K., Bag, S. S., 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.

    Article  CAS  Google Scholar 

  32. Manjit, Yadav, A., Aggarwal, N. K., Kumar, K., & Kumar, A. (2008). Tannase production by Aspergillus fumigatus MA under solid-state fermentation. World J Microbiol Biotechnol, 24, 3023–3030.

    Article  CAS  Google Scholar 

  33. Mata-Gomez, M. A., Rodríguez, L. V., Ramos, E. L., Renovato, J., Cruz-Hernández, M. A., Rodríguez, R., et al. (2009). A novel tannase from the xerophilic fungus Aspergillus niger GH1. J Microbiol Biotechnol, 19, 987–996.

    Article  Google Scholar 

  34. Mohanasrinivasan, V., Dhrisya, P., Dipinsha, K. P., Unnithan, C. M., Viswanath, K. M., & Devi, C. S. (2009). A comparative study of the lipase yield by solid state and submerged fermentations using fungal species from biopharmaceutical oil waste. Afr J Biotechnol, 8, 73–76.

    CAS  Google Scholar 

  35. Mondal, K. C., & Pati, B. R. (2000). Studies on the extracellular tannase from newly isolated Bacillus licheniformis KBR 6. J Basic Microbiol, 40, 223–232.

    Article  CAS  Google Scholar 

  36. Natarajan, K., & Rajendran, A. (2009). Effect of fermentation parameters on extra cellular tannase production by Lactobacillus plantarum MTCC 1407. E J Chem, 6, 979–984.

    CAS  Google Scholar 

  37. Prasad D, Gupta RK, Naidu RB, Kamini NR, Gowthaman MK (2008) Solid state fermentation of tannase from a new Aspergillus isolate. 49th Annual Conference of Association of Microbiologists of India. New Delhi, India.

  38. Rajakumar, G., & Nandy, S. C. (1983). Isolation, purification, and some properties of Penicillium chrysogenum tannase. Appl Environ Microbiol, 46, 525–527.

    CAS  Google Scholar 

  39. Ramírez-Coronel, M. A., Viniegra-González, G., Darvill, A., & Augur, C. (2003). A novel tannase from Aspergillus niger with β-glucosidase activity. Microbiology, 149, 2941–2946.

    Article  Google Scholar 

  40. Rana, N. K., & Bhat, T. K. (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.

    Article  CAS  Google Scholar 

  41. 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.

    Article  Google Scholar 

  42. Saqib, A. A. N., Hassan, M., Khan, N. F., & Baig, S. (2010). Thermostability of crude endoglucanase from Aspergillus fumigatus grown under solid state fermentation (SSF) and submerged fermentation (SmF). Process Biochem, 45, 641–646.

    Article  CAS  Google Scholar 

  43. Sharma, S., Bhat, T. K., & Dawra, R. K. (1999). Isolation, purification and properties of tannase from Aspergillus niger van Tieghem. World J Microbiol Biotechnol, 15, 673–677.

    Article  CAS  Google Scholar 

  44. Sharma, S., & Gupta, M. N. (2003). Synthesis of antioxidant propyl gallate using tannase from Aspergillus niger van Teighem in nonaqueous media. Bioorg Med Chem Lett, 13, 395–397.

    Article  CAS  Google Scholar 

  45. Strumeyer, D. H., & Malin, M. J. (1970). Resistance of extracellular yeast invertase and other glycoproteins to denaturation by tannins. Biochem J, 118, 899–900.

    CAS  Google Scholar 

  46. Taşkın, E., & Stratilová, E. (2008). Polygalacturonases produced under solid state and submerged fermentation conditions by two strains of Aspergillus foetidus. Turk J Biochem, 33, 190–196.

    Google Scholar 

  47. Vaquero, I., Marcobal, A., & Muñoz, R. (2004). Tannase activity by lactic acid bacteria isolated from grape must and wine. Int J Food Microbiol, 96, 199–204.

    Article  CAS  Google Scholar 

  48. Viniegra-González, G., Favela-Torres, E., Aguilar, C., Romero-Gomez, S. D. J., Díaz-Godínez, G., & Augur, C. (2003). Advantages of fungal enzyme production in solid state over liquid fermentation systems. Biochem Eng J, 13, 157–167.

    Article  Google Scholar 

  49. Yamada, K., Iibuchi, S., & Minoda, Y. (1968). Studies on tannin acyl hydrolase of microorganisms. Isolation and identification of producing molds and studies on the conditions of cultivation. Agric Biol Chem, 45, 233–240.

    Google Scholar 

  50. Yu, X. W., & Li, Y. Q. (2006). Kinetics and thermodynamics of synthesis of propyl gallate by mycelium-bound tannase from Aspergillus niger in organic solvent. J Mol Catal B Enzym, 40, 44–50.

    Article  CAS  Google Scholar 

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Acknowledgments

Jaqueline Renovato and Luis Rodríguez-Durán thank the National Council on Science and Technology (CONACYT), Mexico for the post-graduate scholarship.

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Authors and Affiliations

  1. Food Research Department, School of Chemistry, Universidad Autónoma de Coahuila, Blvd. V. Carranza and González Lobo, ZIP 25280, Saltillo, Coahuila, Mexico

    Jaqueline Renovato, Luis V. Rodríguez-Durán, Raúl Rodríguez & Cristóbal Noe Aguilar

  2. Complex Carbohydrate Research Center, University of Georgia, 315 Riverbend Road, Athens, GA, 30602-4712, USA

    Gerardo Gutiérrez-Sánchez & Carl Bergman

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  1. Jaqueline Renovato
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  2. Gerardo Gutiérrez-Sánchez
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  3. Luis V. Rodríguez-Durán
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  6. Cristóbal Noe Aguilar
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Correspondence to Cristóbal Noe Aguilar.

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Renovato, J., Gutiérrez-Sánchez, G., Rodríguez-Durán, L.V. et al. Differential Properties of Aspergillus niger Tannase Produced Under Solid-State and Submerged Fermentations. Appl Biochem Biotechnol 165, 382–395 (2011). https://doi.org/10.1007/s12010-011-9258-3

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