Skip to main content
SpringerLink
Log in

Highly Efficient Extraction of Ferulic Acid from Cereal Brans by a New Type A Feruloyl Esterase from Eupenicillium parvum in Combination with Dilute Phosphoric Acid Pretreatment

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Feruloyl esterase (FAE) is a critical enzyme in bio-extraction of ferulic acid (FA) from plant cell wall. A new FAE (EpFAE1) encoding gene was isolated from Eupenicillium parvum and heterologously expressed in Pichia pastoris cells. Based on phylogenetic tree analysis, the protein EpFAE1 belongs to type A of the seventh FAE subfamily. Using methyl ferulate as substrate, the optimum temperature and pH for the catalytic activity of EpFAE1 were 50 °C and 5.5, respectively. The enzyme exhibited high stability at 50 °C, in a wide pH range (3.0–11.0), or in the presence of 2 M of NaCl. Together with the endo-xylanase EpXYN1, EpFAE1 released 72.32% and 4.00% of the alkali-extractable FA from de-starched wheat bran (DSWB) or de-starched corn bran (DSCB), respectively. Meanwhile, the substrates were pretreated with 1.75% (for DSWB) or 1.0% (for DSCB) of phosphoric acid (PA) at 90 °C for 12 h, followed by enzymatic hydrolysis of the soluble and insoluble fractions. The release efficiencies of FA were up to 84.64% for DSWB and 66.73% for DSCB. Combined dilute PA pretreatment with enzymatic hydrolysis is a low-cost and highly efficient method for the extraction of FA from cereal brans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

FAE:

feruloyl esterase (ferulic acid esterase)

MFA:

methyl ferulate

FA:

ferulic acid

SDS-PAGE:

sodium dodecyl sulfate-polyacrylamide gel electrophoresis

DSWB:

de-starched wheat bran

DSCB:

de-starched corn bran

PA:

phosphoric acid

HPLC:

high-performance liquid chromatography

MW:

molecular weight

References

  1. Oliveira, D. M., Mota, T. R., Oliva, B., Segato, F., Marchiosi, R., Ferrarese-Filho, O., Faulds, C. B., & Dos Santos, W. D. (2019). Feruloyl esterases: Biocatalysts to overcome biomass recalcitrance and for the production of bioactive compounds. Bioresource Technology, 278, 408–423.

    Article  CAS  PubMed  Google Scholar 

  2. Dilokpimol, A., Makela, M. R., Aguilar-Pontes, M. V., Benoit-Gelber, I., Hilden, K. S., & de Vries, R. P. (2016). Diversity of fungal feruloyl esterases: updated phylogenetic classification, properties, and industrial applications. Biotechnology for Biofuels, 9, 231.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  3. Crepin, V. F., Faulds, C. B., & Connerton, I. F. (2004). Functional classification of the microbial feruloyl esterases. Applied Microbiology and Biotechnology, 63(6), 647–652.

    Article  CAS  PubMed  Google Scholar 

  4. Gopalan, N., Rodriguez-Duran, L. V., Saucedo-Castaneda, G., & Nampoothiri, K. M. (2015). Review on technological and scientific aspects of feruloyl esterases: A versatile enzyme for biorefining of biomass. Bioresource Technology, 193, 534–544.

    Article  CAS  PubMed  Google Scholar 

  5. Udatha, D. B., Kouskoumvekaki, I., Olsson, L., & Panagiotou, G. (2011). The interplay of descriptor-based computational analysis with pharmacophore modeling builds the basis for a novel classification scheme for feruloyl esterases. Biotechnology Advances, 29(1), 94–110.

    Article  CAS  PubMed  Google Scholar 

  6. Kumar, N., & Pruthi, V. (2014). Potential applications of ferulic acid from natural sources. Biotechnology Reports, 4, 86–93.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Chandrasekharaiah, M., Thulasi, A., Bagath, M., Kumar, D. P., Santosh, S. S., Palanivel, C., Jose, V. L., & Sampath, K. T. (2011). Molecular cloning, expression and characterization of a novel feruloyl esterase enzyme from the symbionts of termite(Coptotermes formosanus) gut. BMB Reports, 44(1), 52–57.

    Article  CAS  PubMed  Google Scholar 

  8. Dilokpimol, A., Makela, M. R., Varriale, S., Zhou, M., Cerullo, G., Gidijala, L., Hinkka, H., Bras, J. L. A., Jutten, P., Piechot, A., Verhaert, R., Hildén, K. S., Faraco, V., & de Vries, R. P. (2018). Fungal feruloyl esterases: Functional validation of genome mining based enzyme discovery including uncharacterized subfamilies. New Biotechnology, 41, 9–14.

    Article  CAS  PubMed  Google Scholar 

  9. Chen, X., Guo, Y., Jia, G., Zhao, H., Liu, G., & Huang, Z. (2019). Ferulic acid regulates muscle fiber type formation through the Sirt1/AMPK signaling pathway. Food&Function, 10(1), 259–265.

    CAS  Google Scholar 

  10. Shirai, A., Watanabe, T., & Matsuki, H. (2017). Inactivation of foodborne pathogenic and spoilage micro-organisms using ultraviolet-A light in combination with ferulic acid. Letters in Applied Microbiology, 64(2), 96–102.

    Article  CAS  PubMed  Google Scholar 

  11. Ranum, P., Pena-Rosas, J. P., & Garcia-Casal, M. N. (2014). Global maize production, utilization, and consumption. Annals of the New York Academy of Sciences, 1312, 105–112.

    Article  PubMed  Google Scholar 

  12. Bento-Silva, A., Vaz Patto, M. C., & do Rosario Bronze M. (2018). Relevance, structure and analysis of ferulic acid in maize cell walls. Food Chemistry, 246, 360–378.

    Article  CAS  PubMed  Google Scholar 

  13. Wang, L., Ma, Z., Du, F., Wang, H., & Ng, T. B. (2014). Feruloyl esterase from the edible mushroom Panus giganteus: a potential dietary supplement. Journal of Agricultural and Food Chemistry, 62(31), 7822–7827.

    Article  CAS  PubMed  Google Scholar 

  14. Topakas, E., Vafiadi, C., & Christakopoulos, P. (2007). Microbial production, characterization and applications of feruloyl esterases. Process Biochemistry, 42(4), 497–509.

    Article  CAS  Google Scholar 

  15. Levasseur, A., Navarro, D., Punt, P. J., Belaich, J. P., Asther, M., & Record, E. (2005). Construction of engineered bifunctional enzymes and their overproduction in Aspergillus niger for improved enzymatic tools to degrade agricultural by-products. Applied and Environmental Microbiology, 71(12), 8132–8140.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Wu, H., Li, H., Xue, Y., Luo, G., Gan, L., Liu, J., Mao, L., & Long, M. (2017). High efficiency co-production of ferulic acid and xylooligosaccharides from wheat bran by recombinant xylanase and feruloyl esterase. Biochemical Engineering Journal, 120, 41–48.

    Article  CAS  Google Scholar 

  17. Agger, J., Vikso-Nielsen, A., & Meyer, A. S. (2010). Enzymatic xylose release from pretreated corn bran arabinoxylan: differential effects of deacetylation and deferuloylation on insoluble and soluble substrate fractions. Journal of Agricultural and Food Chemistry, 58(10), 6141–6148.

    Article  CAS  PubMed  Google Scholar 

  18. Zhou, X., & Xu, Y. (2019). Integrative process for sugarcane bagasse biorefinery to co-produce xylooligosaccharides and gluconic acid. Bioresource Technology, 282, 81–87.

    Article  CAS  PubMed  Google Scholar 

  19. Amnuaycheewa, P., Hengaroonprasan, R., Rattanaporn, K., Kirdponpattara, S., Cheenkachorn, K., & Sriariyanun, M. (2016). Enhancing enzymatic hydrolysis and biogas production from rice straw by pretreatment with organic acids. Industrial Crops and Products, 87, 247–254.

    Article  CAS  Google Scholar 

  20. Kundu, C., & Lee, J. W. (2016). Bioethanol production from detoxified hydrolysate and the characterization of oxalic acid pretreated Eucalyptus (Eucalyptus globulus) biomass. Industrial Crops and Products, 83, 322–328.

    Article  CAS  Google Scholar 

  21. Nair, R. B., Kalif, M., Ferreira, J. A., Taherzadeh, M. J., & Lennartsson, P. R. (2017). Mild-temperature dilute acid pretreatment for integration of first and second generation ethanol processes. Bioresource Technology, 245, 145–151.

    Article  CAS  PubMed  Google Scholar 

  22. Nair, R. B., Lundin, M., Brandberg, T., Lennartsson, P. R., & Taherzadeh, M. J. (2015). Dilute phosphoric acid pretreatment of wheat bran for enzymatic hydrolysis and subsequent ethanol production by edible fungi Neurospora intermedia. Industrial Crops and Products, 69, 314–323.

    Article  CAS  Google Scholar 

  23. Dilokpimol, A., Makela, M. R., Mansouri, S., Belova, O., Waterstraat, M., Bunzel, M., de Vries, R. P., & Hilden, K. S. (2017). Expanding the feruloyl esterase gene family of Aspergillus niger by characterization of a feruloyl esterase, FaeC. New Biotechnology, 37(Pt B), 200–209.

    Article  CAS  PubMed  Google Scholar 

  24. Li, X., Guo, J., Hu, Y., Yang, Y., Jiang, J., Nan, F., Wu, S., & Xin, Z. (2019). Identification of a novel feruloyl esterase by functional screening of a soil metagenomic library. Applied Biochemistry and Biotechnology, 187(1), 424–437.

    Article  CAS  PubMed  Google Scholar 

  25. Uraji, M., Tamura, H., Mizohata, E., Arima, J., Wan, K., Ogawa, K., Inoue, T., & Hatanaka, T. (2018). Loop of Streptomyces feruloyl esterase plays an important role in the enzyme's catalyzing the release of ferulic acid from biomass. Applied and Environmental Microbiology, 84(3), e02300–e02317.

    Article  PubMed Central  PubMed  Google Scholar 

  26. Long, L., Ding, D., Han, Z., Zhao, H., Lin, Q., & Ding, S. (2016). Thermotolerant hemicellulolytic and cellulolytic enzymes from Eupenicillium parvum 4-14 display high efficiency upon release of ferulic acid from wheat bran. Journal of Applied Microbiology, 121(2), 422–434.

    Article  CAS  PubMed  Google Scholar 

  27. Jiang, K., Li, L., Long, L., & Ding, S. (2018). Comprehensive evaluation of combining hydrothermal pretreatment (autohydrolysis) with enzymatic hydrolysis for efficient release of monosaccharides and ferulic acid from corn bran. Industrial Crops and Products, 113, 348–357.

    Article  CAS  Google Scholar 

  28. Long, L., Xu, M., Shi, Y., Lin, Q., Wang, J., & Ding, S. (2018). Characterization of two new endo-beta-1,4-xylanases from Eupenicillium parvum 4-14 and their applications for production of feruloylated oligosaccharides. Applied Biochemistry and Biotechnology, 186(4), 816–833.

    Article  CAS  PubMed  Google Scholar 

  29. Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Robert, X., & Gouet, P. (2014). Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Research, 42(Web Server issue), W320–W324.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Gong, Y. Y., Yin, X., Zhang, H. M., Wu, M. C., Tang, C. D., Wang, J. Q., & Pang, Q. F. (2013). Cloning, expression of a feruloyl esterase from Aspergillus usamii E001 and its applicability in generating ferulic acid from wheat bran. Journal of Industrial Microbiology & Biotechnology, 40(12), 1433–1441.

    Article  CAS  Google Scholar 

  32. de Vries, R. P., Michelsen, B., Poulsen, C. H., Kroon, P. A., van den Heuvel, R. H., Faulds, C. B., Williamson, G., van den Hombergh, J. P., & Visser, J. (1997). The faeA genes from Aspergillus niger and Aspergillus tubingensis encode ferulic acid esterases involved in degradation of complex cell wall polysaccharides. Applied and Environmental Microbiology, 63(12), 4638–4644.

    Article  PubMed Central  PubMed  Google Scholar 

  33. Nieter, A., Kelle, S., Linke, D., & Berger, R. G. (2016). Feruloyl esterases from Schizophyllum commune to treat food industry side-streams. Bioresource Technology, 220, 38–46.

    Article  CAS  PubMed  Google Scholar 

  34. Long, L., Zhao, H., Ding, D., Xu, M., & Ding, S. (2018). Heterologous expression of two Aspergillus niger feruloyl esterases in Trichoderma reesei for the production of ferulic acid from wheat bran. Bioprocess and Biosystems Engineering, 41(5), 593–601.

    Article  CAS  PubMed  Google Scholar 

  35. Ewert, J., Gluck, C., Strasdeit, H., Fischer, L., & Stressler, T. (2018). Influence of the metal ion on the enzyme activity and kinetics of PepA from Lactobacillus delbrueckii. Enzyme and Microbial Technology, 110, 69–78.

    Article  CAS  PubMed  Google Scholar 

  36. Uraji, M., Arima, J., Inoue, Y., Harazono, K., & Hatanaka, T. (2014). Application of two newly identified and characterized feruloyl esterases from Streptomyces sp. in the enzymatic production of ferulic acid from agricultural biomass. PLoS One, 9(8), e104584.

    Article  PubMed Central  PubMed  Google Scholar 

  37. Zeng, Y., Yin, X., Wu, M. C., Yu, T., Feng, F., Zhu, T. D., & Pang, Q. F. (2014). Expression of a novel feruloyl esterase from Aspergillus oryzae in Pichia pastoris with esterification activity. Journal of Molecular Catalysis B: Enzymatic, 110, 140–146.

    Article  CAS  Google Scholar 

  38. Hunt, C. J., Tanksale, A., & Haritos, V. S. (2016). Biochemical characterization of a halotolerant feruloyl esterase from Actinomyces spp.: refolding and activity following thermal deactivation. Applied Microbiology and Biotechnology, 100(4), 1777–1787.

    Article  CAS  PubMed  Google Scholar 

  39. Yu, P., Maenz, D. D., McKinnon, J. J., Racz, V. J., & Christensen, D. A. (2002). Release of ferulic acid from oat hulls by Aspergillus ferulic acid esterase and Trichoderma xylanase. Journal of Agricultural and Food Chemistry, 50(6), 1625–1630.

    Article  CAS  PubMed  Google Scholar 

  40. Feher, C., Gal, B., Feher, A., Barta, Z., & Reczey, K. (2015). Investigation of commercial enzyme preparations for selective release of arabinose from corn fibre. Journal of Chemical Technology and Biotechnology, 90(7), 1329–1337.

    Article  CAS  Google Scholar 

  41. Agger, J., Johansen, K. S., & Meyer, A. S. (2011). pH catalyzed pretreatment of corn bran for enhanced enzymatic arabinoxylan degradation. New Biotechnology, 28(2), 125–135.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Franz St. John from the USDA Forest Service for improving the manuscript.

Funding

This work was supported by grants from a 948 Research Project (No. 2013-4-16) from the State Forestry Administration of China, a research project (30370043) from the National Natural Science Foundation of China, the Jiangsu Provincial Government Scholarship for Overseas Studies from Jiangsu Provincial Department of Education, China, a Science and Technology Project of Guizhou Province in China (Grant No. [2019]2333), and the Priority Academic Program Development of Jiangsu Higher Education Institutions.

Author information

Author notes

  1. Liangkun Long and Lianqiu Wu contributed equally to this work.

Authors and Affiliations

  1. College of Chemical Engineering, Nanjing Forestry University, Nanjing, 210037, China

    Liangkun Long, Lianqiu Wu & Shaojun Ding

  2. Jiangsu Co-Innovation Center of Efficient Processing and Utilization of Forest Resources, Nanjing Forestry University, Nanjing, 210037, China

    Liangkun Long & Shaojun Ding

  3. Jiangsu Key Lab for the Chemistry & Utilization of Agricultural and Forest Biomass, Nanjing, 210037, China

    Liangkun Long & Shaojun Ding

  4. Nanjing Institute for the Comprehensive Utilization of Wild Plants, Nanjing, 211111, China

    Qunying Lin

Authors
  1. Liangkun Long
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lianqiu Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qunying Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shaojun Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shaojun Ding.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 1037 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Long, L., Wu, L., Lin, Q. et al. Highly Efficient Extraction of Ferulic Acid from Cereal Brans by a New Type A Feruloyl Esterase from Eupenicillium parvum in Combination with Dilute Phosphoric Acid Pretreatment. Appl Biochem Biotechnol 190, 1561–1578 (2020). https://doi.org/10.1007/s12010-019-03189-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-019-03189-6

Keywords

Search

Navigation