Journal of Food Science and Technology

, Volume 54, Issue 3, pp 778–785 | Cite as

Enrichment of maize and triticale bran with recombinant Aspergillus tubingensis ferulic acid esterase

  • Eunice N. Zwane
  • Petrus J. van Zyl
  • Kwaku G. Duodu
  • Shaunita H. Rose
  • Karl Rumbold
  • Willem H. van Zyl
  • Marinda Viljoen-Bloom
Original Article

Abstract

Ferulic acid is a natural antioxidant found in various plants and serves as a precursor for various fine chemicals, including the flavouring agent vanillin. However, expensive extraction methods have limited the commercial application of ferulic acid, in particular for the enrichment of food substrates. A recombinant Aspergillus tubingensis ferulic acid esterase Type A (FAEA) was expressed in Aspergillus niger D15#26 and purified with anion-exchange chromatography (3487 U/mg, K m  = 0.43 mM, K cat = 0.48/min on methyl ferulate). The 36-kDa AtFAEA protein showed maximum ferulic acid esterase activity at 50 °C and pH 6, suggesting potential application in industrial processes. A crude AtFAEA preparation extracted 26.56 and 8.86 mg/g ferulic acid from maize bran and triticale bran, respectively, and also significantly increased the levels of p-coumaric and caffeic acid from triticale bran. The cost-effective production of AtFAEA could therefore allow for the enrichment of brans generally used as food and fodder, or for the production of fine chemicals (such as ferulic and p-coumaric acid) from plant substrates. The potential for larger-scale production of AtFAEA was demonstrated with the A. niger D15[AtfaeA] strain yielding a higher enzyme activity (185.14 vs. 83.48 U/ml) and volumetric productivity (3.86 vs. 1.74 U/ml/h) in fed-batch than batch fermentation.

Keywords

Ferulic acid esterase Aspergillus niger Aspergillus tubingensis Triticale Maize 

Notes

Acknowledgements

This work is based on the research supported in part by the National Research Foundation of South Africa (Grant 76597 to MVB and Grant 86423 to WHvZ). Prof Peter Punt, TNO Microbiology and Systems Biology, Netherlands, kindly provided the Aspergillus niger D15#26 host strain.

Author’s contribution

ENZ was the principal researcher responsible for experimental planning, execution, data collection and analyses, as well as drafting the manuscript. PJvZ assisted with the fermentation protocol; KGD with bran treatments and chemical analyses; SHR and KR with enzyme characterisation. WHvZ provided intellectual input together with MVB who prepared the final manuscript with all authors participating in the final editing.

References

  1. Balasundram N, Sundram K, Samman S (2006) Phenolic compounds in plants and agri-industrial by-products: antioxidant activity, occurrence, and potential uses. Food Chem 99:191–203CrossRefGoogle Scholar
  2. Benoit I, Navarro D, Marnet N, Rakotomanomana N, Lesage-Meessen L, Sigoillot JC, Asther M (2006) Feruloyl esterase as a tool for the release of phenolic compounds from agro-industrial by-products. Carbohydr Res 341:1820–1827CrossRefGoogle Scholar
  3. Benoit I, Danchin EGJ, Bleichrodt RJ, de Vries RP (2008) Biotechnological applications and potential of fungal feruloyl esterases based on prevalence, classification and biochemical diversity. Biotechnol Lett 30:387–396CrossRefGoogle Scholar
  4. De Vries RP, Michelser B, Poulsen CH, Kroon PA, van den Heuvel RH, Faulds CB, Williamson G, van den Hombergh JP, Visser J (1997) The faeA genes from Aspergillus niger and Aspergillus tubingensis encodes ferulic acid esterases involved in degradation of complex cell wall polysaccharides. Appl Environ Microbiol 63:4638–4644Google Scholar
  5. De Vries RP, Kester HCM, van Kuyk PA (2002) The Aspergillus niger faeB gene encodes a second feruloyl esterase involved in pectin and xylan degradation, and is specifically induced on aromatic compounds. Biochem J 363:377–386CrossRefGoogle Scholar
  6. Debeire P, Khoune P, Jeltsch J-M, Phalip V (2012) Product patterns of a feruloyl esterase from Aspergillus nidulans on large feruloyl-arabino-xylo-oligosaccharides from wheat bran. Bioresour Technol 119:425–428CrossRefGoogle Scholar
  7. Faulds CB, Williamson G (1993) Ferulic acid esterase from Aspergillus niger: purification and partial characterisation of two forms from a commercial source of pectinase. Biotechnol Appl Biochem 17:349–359Google Scholar
  8. Faulds CB, de Vries R, Visser J, Williamson G (1998) Stability of feruloyl esterases from Aspergillus. Biochem Soc T 26:S165CrossRefGoogle Scholar
  9. Fazary AE, Ju YH (2007) Feruloyl esterase as biotechnological tools: current and future perspective. Acta Biochim Biophys Sin 39:811–828CrossRefGoogle Scholar
  10. Fazary AE, Ju YH (2008) The large-scale use of feruloyl esterases in industry. Biotechnol Mol Biol Rev 3:095–110Google Scholar
  11. Gong YY, Yin X, Zhang HM, Wu MC, Tang CD, Wang JQ, Pang QF (2013) Cloning, expression of a feruloyl esterase from Aspergillus usamii E001 and its applicability in generating ferulic acid from wheat bran. J Ind Microbiol Biotechnol 40:1433–1441CrossRefGoogle Scholar
  12. Graf E (1992) Antioxidant potential of ferulic acid. Free Radical Biol Med 13:435–448CrossRefGoogle Scholar
  13. Hedge S, Srinivas P, Muralikrishna G (2009) Single-step synthesis of 4-nitrophenyl ferulate for spectrophotometric assay of feruloylesterase. Anal Biochem 387:128–129CrossRefGoogle Scholar
  14. Heinonen M, Rein D, Satue-Gracia MT, Huang SW, German JB, Frankel EN (1998) Effect of protein on the antioxidant activity of phenolic compounds in a lecithin-liposome oxidation system. J Agr Food Chem 46:917–922CrossRefGoogle Scholar
  15. Hosseinian FS, Mazza G (2009) Triticale bran and straw: potential new sources of phenolic acids, proanthocyanidins, and lignans. J Funct Foods 1:57–64CrossRefGoogle Scholar
  16. Kanauchi M, Watanabe S, Tsukada T, Atta K, Kakuta T, Koizumi T (2008) Purification and characterisation of ferulyol esterase from Aspergillus awamori G-2 strain. J Food Sci 73:458–463CrossRefGoogle Scholar
  17. Kim M, Hyun J, Kim J, Park J, Kim M, Kim J, Lee S, Chun S, Chung F (2007) Relationship between phenolic compounds, anthocyanins content and antioxidant activity in colored barley germplasm. J Agr Food Chem 55:4802–4809CrossRefGoogle Scholar
  18. Koseki T, Takahashi K, Fushinobu S, Iefuji H, Iwano K, Hashizume K, Matsuzawa H (2005) Mutational analysis of a feruloyl esterase from Aspergillus awamori involved in substrate discrimination and pH dependence. Biochim Biophys Acta 1722:200–208CrossRefGoogle Scholar
  19. Koseki T, Takahashi K, Handa T, Yamane Y, Fushinobu S, Hashizume K (2006) N-Linked oligosaccharides of Aspergillus awamori feruloyl esterase are important for thermostability and catalysis. Biosci Biotechnol Biochem 70:2476–2480CrossRefGoogle Scholar
  20. Koseki T, Fushinobu S, Ardiansyah SH, Komai M (2009) Occurrence, properties, and applications of feruloyl esterases. Appl Microbiol Biotechnol 84:803–810CrossRefGoogle Scholar
  21. Kumar N, Pruthi V (2014) Potential applications of ferulic acid from natural sources. Biotechnol Rep 4:86–93CrossRefGoogle Scholar
  22. Lapierre C, Pollet B, Ralet M, Saulnier L (2001) The phenolic fraction of maize bran: evidence for lignin-heteroxylan association. Phytochemistry 57:765–772CrossRefGoogle Scholar
  23. Mathew S, Abraham TE (2004) Ferulic acid: an antioxidant found naturally in plant cell walls and feruloyl esterases involved in its release and their applications. Crit Rev Biotechnol 24:59–83CrossRefGoogle Scholar
  24. Poidevin L, Levasseur A, Pae G, Navarro D, Heiss-Blanquet S, Asther M, Record E (2009) Heterologous production of the Piromyces equi cinnamoyl esterase in Trichoderma reesei for biotechnological applications. Lett Appl Microbiol 49:673–678CrossRefGoogle Scholar
  25. Priefert H, Rabenhorst J, Steinbuchel A (2001) Biotechnological production of vanillin. Appl Microbiol Biotechnol 56:296–314CrossRefGoogle Scholar
  26. Rose SH, van Zyl WH (2002) Constitutive expression of the Trichoderma reesei β-1,4-xylanase gene (xyn2) and the β-1,4-endoglucanase gene (egI) in Aspergillus niger in molasses and defined glucose media. Appl Microbiol Biotechnol 58:461–468CrossRefGoogle Scholar
  27. Rose SH, van Zyl WH (2008) Exploitation of Aspergillus niger for the heterologous production of cellulases and hemicelluloses. Open Biotechnol J 2:165–175CrossRefGoogle Scholar
  28. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New YorkGoogle Scholar
  29. Shin H, Chen RR (2006) Production and characterisation of a type B feruloyl esterase from Fusarium proliferatum NRRL 26517. Enzyme Microb Technol 38:478–485CrossRefGoogle Scholar
  30. Sundberg M, Poutanen K, Markkanen P, Linko M (1990) An extracellular esterase of Aspergillus awamori. Biotechnol Appl Biochem 12:670–680Google Scholar
  31. Yu P, McKinnon JJ, Christensen DA (2005) Improving the nutritional value of oat hulls for ruminant animals with pretreatment of a multi-enzyme cocktail: in vitro studies. J Anim Sci 83:1133–1141CrossRefGoogle Scholar
  32. Zhao Z, Moghadasian MH (2008) Chemistry, natural sources, dietary intake and pharmacokinetic properties of ferulic acid: a review. Food Chem 109:691–702CrossRefGoogle Scholar
  33. Zhao S, Yao S, Ou S, Line J, Wang Y, Peng X, Li A, Yu B (2014) Preparation of ferulic acid from corn bran: its improved extraction and purification by membrane separation. Food Bioprod Process 92:309–313CrossRefGoogle Scholar
  34. Zwane EN, Rose SH, van Zyl WH, Rumbold K, Viljoen-Bloom M (2014) Over-expression of Aspergillus tubingensis faeA in protease-deficient Aspergillus niger enables ferulic acid production from plant material. J Ind Microbiol Biotechnol 41:1027–1034CrossRefGoogle Scholar

Copyright information

© Association of Food Scientists & Technologists (India) 2017

Authors and Affiliations

  • Eunice N. Zwane
    • 1
  • Petrus J. van Zyl
    • 2
  • Kwaku G. Duodu
    • 3
  • Shaunita H. Rose
    • 1
  • Karl Rumbold
    • 4
  • Willem H. van Zyl
    • 1
  • Marinda Viljoen-Bloom
    • 1
  1. 1.Department of MicrobiologyStellenbosch UniversityMatielandSouth Africa
  2. 2.CSIR BiosciencesPretoriaSouth Africa
  3. 3.Department of Food ScienceUniversity of PretoriaHatfield, PretoriaSouth Africa
  4. 4.School of Molecular and Cell BiologyUniversity of the Witwatersrand (WITS)WitsSouth Africa

Personalised recommendations