Skip to main content
SpringerLink
Log in

Solid-state fermentation of Ginkgo biloba L. residue for optimal production of cellulase, protease and the simultaneous detoxification of Ginkgo biloba L. residue using Candida tropicalis and Aspergillus oryzae

  • Original Paper
  • Published:
European Food Research and Technology Aims and scope Submit manuscript

Abstract

Ginkgo biloba L. residue (GBLR) is a by-product generated from flavonoids extraction of G. biloba L. Although it contains a high amount of nutritive components, it has toxic compound of ginkgolic acids which restricts its application in the food or animal feed industries. Also, the disposal of huge quantity of GBLR is a major environmental problem in the future. This study investigated the potential of a utilization of GBLR as substrate for cellulase and protease productions by solid-state fermentation (SSF) with Candida tropicalis and Aspergillus oryzae. The study simultaneously is focused on the biodetoxification of toxins in GBLR. The optimum SSF conditions for enzyme production were evaluated as, supplementation with 2 % maltose and peptone, inoculation with 1 × 107 fungi per 5 g residues, 7.0 pH, 40 % moisture content, 25 °C incubation temperature, and 4 days incubation time. Under these conditions, cellulase and protease activities reached up to 1,168.26 and 3,145.68 U/g, respectively. The main toxic compound ginkgolic acid content in the GBLR was reduced from 14.8 to 1.5 mg/g after SSF. The cytotoxicity of the fermented GBLR evaluated by methyl thiazolyl tetrazolium testing on abelson murine leukemia virus-induced tumor cells showed almost 100 % of cellular viability after 4 days of fermentation. Our results indicate that SSF of GBLR could produce industrial enzymes and the detoxified fermented GBLR could be potentially applied to animal feed.

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

Similar content being viewed by others

References

  1. Jacobs BP, Browner WS (2000) Ginkgo biloba: a living fossil. Am J Med 108:341–342

    Article  CAS  Google Scholar 

  2. Li H, Zhou GY, Xu JP, Liu JA, Zhang HY, Tan YM (2012) Research progress on polysaccharides from Ginkgo biloba. J Med Plants Res 6:171–176

    Article  CAS  Google Scholar 

  3. Van-Beek TA, Montoro P (2009) Chemical analysis and quality control of Ginkgo biloba leaves, extracts, and phytopharmaceuticals. J Chromatogr A 1216:2002–2032

    Article  CAS  Google Scholar 

  4. Liu ZH, Zeng S (2009) Cytotoxicity of ginkgolic acid in HepG2 cells and primary rat hepatocytes. Toxicol Lett 187:131–136

    Article  CAS  Google Scholar 

  5. Kuhad RC, Singh A, Eriksson KEL (1997) Microorganisms and enzymes involved in the degradation of plant fibre cell wall. Adv Biochem Biotechnol 57:47–125

    Google Scholar 

  6. Li H, Liang WQ, Wang ZY, Luo N, Wu XY, Hu JM, Lu JQ, Zhang XY, Wu PC, Liu YH (2006) Enhanced production and partial characterization of thermostable α-galactosidase by thermotolerant Absidia sp. WL511 in solid state fermentation using response surface methodology. World J Microbiol Biotechnol 22:1–7

    Article  Google Scholar 

  7. Basu S, Gaur R, Gomes J, Sreekrishnan TR, Bisaria VS (2002) Effect of seed culture on solid state bioconversion of wheat straw by Phanerochaete chrysosporium for animal feed. J Biosci Bioeng 93:25–30

    Article  CAS  Google Scholar 

  8. Rudravaram R, Chandel AK, Linga VR, Pogaku R (2006) Optimization of protein enrichment of deoiled rice bran by solid state fermentation using Aspergillus oryzae MTCC 1846. Int J Food Eng 2:1–14

    Article  Google Scholar 

  9. Ravinder R, Linga VR, Pogaku R (2003) Production of SCP from deoiled rice bran. Food Technol Biotechnol 41:243–246

    CAS  Google Scholar 

  10. Godoy MG, Gutarra MLE, Maciel FM, Felix SP, Bevilaqua JV, Machado OLT, Freire DMG (2009) Use of a low-cost methodology for biodetoxification of castor bean waste and lipase production. Enzyme Microbiol Technol 44:317–322

    Article  CAS  Google Scholar 

  11. Li X, Pang Y, Zhang R (2001) Compositional changes of cottonseed hull substrate during P. Ostreatus growth and the effects on the feeding value of the spent substrate. Bioresour Technol 80:157–161

    Article  CAS  Google Scholar 

  12. Okano K, Fukui S, Kitao R, Usagawa T (2007) Effects of culture length of Pleurotus eryngii grown on sugarcane bagasse on in vitro digestibility and chemical composition. Anim Feed Sci Technol 136:240–247

    Article  CAS  Google Scholar 

  13. Brozzoli V, Bartocci S, Terramoccia S, Contò G, Federici FD, Annibale A, Petruccioli M (2010) Stoned olive pomace fermentation with Pleurotus species and its evaluation as a possible animal feed. Enzyme Microb Technol 46:223–228

    Article  CAS  Google Scholar 

  14. Veerabhadrappa MB, Shivakumar SB, Devappa S (2014) Solid-state fermentation of Jatropha seed cake for optimization of lipase, protease and detoxification of anti-nutrients in Jatropha seed cake using Aspergillus versicolor CJS-98. J Biosci Bioeng 117:208–214

    Article  CAS  Google Scholar 

  15. AOAC (1990) Official methods of analysis, 17th edn. Association of Official Analytical Chemists, Gaithersburg

    Google Scholar 

  16. Fuzzati N, Pace R, Villa F (2003) A simple HPLC–UV method for the assay of ginkgolic acids in Ginkgo biloba extracts. Fitoterapia 74:247–256

    Article  CAS  Google Scholar 

  17. Rezaeian M, Beakes GW, Chaudhry AS (2005) Relative fibrolytic activities of anaerobic rumen fungi on untreated and sodium hydroxide treated barley straw in in vitro culture. Ecol Environ Microbiol 11:163–175

    CAS  Google Scholar 

  18. Agrawal D, Partidar P, Banerjee T, Patil S (2005) Alkaline protease production by a soil isolate of Beauveria feline under SSF condition: parameter optimization and application to soy protein hydrolysis. Process Biochem 40:1131–1136

    Article  CAS  Google Scholar 

  19. Lowry OH, Rosebrough NJ, Farr A, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  20. He JR, Xie BJ (2002) Reversed-phase argentation high-performance liquid chromatography in phytochemical analysis of ginkgolic acids in leaves from Ginkgo biloba L. J Chromatogr A 943:303–309

    Article  CAS  Google Scholar 

  21. He XG, Bernart MW, Nolan GS, Lin LZ, Lindenmaier MP (2000) High-performance liquid chromatography–electrospray ionization–mass spectrometry study of ginkgolic acid in the leaves and fruits of the ginkgo tree (Ginkgo biloba). J Chromatogr Sci 38:169–173

    Article  CAS  Google Scholar 

  22. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63

    Article  CAS  Google Scholar 

  23. Hashemi M, Razavi SH, Shojaosadati SA, Mousavi SM, Khajeh K, Safari M (2010) Development of a solid-state fermentation process for production of an alpha amylase with potentially interesting properties. J Biosci Bioeng 110:333–337

    Article  CAS  Google Scholar 

  24. Van-Beek TA, Wintermans MS (2001) Preparative isolation and dual column high-performance liquid chromatography of ginkgolic acids from Ginkgo biloba. J Chromatogr A 930:109–117

    Article  CAS  Google Scholar 

  25. Yalemtesfa B, Alemu T, Santhanam A (2010) Solid substrate fermentation and conversion of orange waste into fungal biomass using Aspergillus niger KA-06 and Chaetomium Spp KC-06. Afr J Microbiol Res 4:1275–1281

    CAS  Google Scholar 

  26. Iqbal HMN, Asgher M, Ahmed I, Hussain S (2010) Media optimization for hyper-production of carboxymethyl cellulase using proximally analyzed agroindustrial residue with Trichoderma harzianum under SSF. Int J Agro Veter Med Sci 4:47–55

    Google Scholar 

  27. Oberoi HS, Chavan Y, Bansal S, Dhillon GS (2010) Production of cellulases through solid-state fermentation using kinnow pulp as a major substrate. Food Bioprocess Technol 4:528–536

    Article  Google Scholar 

  28. Gupta R, Beg QK, Khan S, Chauhan B (2002) An overview on fermentation, downstream processing and properties of microbial proteases. Appl Microbiol Biotechnol 60:381–395

    Article  CAS  Google Scholar 

  29. De-Loecker R, Goossens W, Van-Duppen V, Verwilghen R, De-Loecker W (1993) Osmotic effects of dilution on erythrocytes after freezing and thawing in glycerol-containing buffer. Cryobiology 30:279–285

    Article  CAS  Google Scholar 

  30. Anto H, Trivedi UB, Patel KC (2006) Glucoamylase production by SSF using rice flake manufacturing waste products as substrate. Bioresour Technol 97:1161–1166

    Article  CAS  Google Scholar 

  31. Chandra MS, Viswanath B, Reddy BR (2007) Cellulolytic enzymes on lignocellulosic substrates in solid state fermentation by Aspergillus niger. Indian J Microbiol 47:323–328

    Article  CAS  Google Scholar 

  32. Sandhya C, Sumantha A, Szakacs G, Pandey A (2005) Comparative evaluation of neutral protease production by Aspergillus oryzaein submerged and solid-state fermentation. Process Biochem 40:2689–2694

    Article  CAS  Google Scholar 

  33. Singhania RR, Sukumaran RK, Pillai A, Prema P, Szakacs G, Pandey A (2006) Solid-state fermentation of lignocellulosic substrates for cellulase production by Trichoderma reesei NRRL 11,460. Indian J Biotechnol 5:332–336

    CAS  Google Scholar 

  34. Gautam SP, Bundela PS, Pandey AK, Khan J, Awasthi MK, Sarsaiya S (2011) Optimization for the production of cellulase enzyme from municipal solid waste residue by two novel cellulolytic fungi. Biotechnol Res Int 1:1–8

    Article  Google Scholar 

  35. Kamath P, Subrahmanyam VM, Venkata-Rao J, Vasantha-Raj P (2010) Optimization of cultural conditions for protease production by a fungal species. Indian J Pharm Sci 72:161–166

    Article  CAS  Google Scholar 

  36. Moon SH, Parulekar SJ (1991) A parametric study of protease production in batch and fed-batch cultures of Bacillus firmus. Biotechnol Bioeng 37:467–483

    Article  CAS  Google Scholar 

  37. Mahanta N, Gupta A, Khare SK (2008) Production of protease and lipase by solvent tolerant Pseudomonas aeruginosa PseA in solid-state fermentation using Jatropha curcas seed cake as substrate. Bioresour Technol 99:1729–1735

    Article  CAS  Google Scholar 

  38. Ramachandran S, Singh SK, Larroche C, Soccol CR, Pandey A (2007) Oil cakes and their biotechnological applications—a review. Bioresour Technol 98:2000–2009

    Article  CAS  Google Scholar 

  39. Botella C, Diaz A, de-Ory I, Webb C, Blandino A (2007) Xylanase and pectinase production by Aspergillus awamori on grape pomace in solid state fermentation. Process Biochem 42:98–101

    Article  CAS  Google Scholar 

  40. Smith AD, Holtzapple MT (2011) Investigation of the optimal carbon-nitrogen ratio and carbohydrate–nutrient blend for mixed-acid batch fermentations. Bioresour Technol 102:5976–5987

    Article  CAS  Google Scholar 

  41. Gao J, Weng H, Zhu D, Yuan M, Guan F, Xi Y (2008) Production and characterization of cellulolytic enzymes from the thermoacidophilic fungal Aspergillus terreus M11 under solid-state cultivation of corn stover. Bioresour Technol 99:7623–7629

    Article  CAS  Google Scholar 

  42. Wang Q, Hou Y, Xu Z, Miao J, Li G (2008) Optimization of cold-active protease production by the psychrophilic bacterium Colwellia sp. NJ341 with response surface methodology. Bioresour Technol 99:1926–1931

    Article  CAS  Google Scholar 

  43. Zhang WJ, Xu ZR, Zhao SH, Sun JY, Yang X (2007) Development of a microbial fermentation process for detoxification of gossypol in cottonseed meal. Anim Feed Sci Technol 135:176–186

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the financial support by the Production and Research Project of Jiangsu Province (BY2013014) and the Special Fund of Scientific Research from Chinese Academy of Forestry (CAFYBB2012015).

Conflict of interest

None.

Compliance with Ethics Requirements

This article does not contain any studies with human or animal subjects.

Author information

Authors and Affiliations

  1. Institute of Chemical Industry of Forest Products, CAF, Nanjing, 210042, Jiangsu, China

    Hao Zhou, Cheng-Zhang Wang, Jian-Zhong Ye, Hong-Xia Chen, Ran Tao & Yu-Si Zhang

Authors
  1. Hao Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cheng-Zhang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jian-Zhong Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hong-Xia Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ran Tao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yu-Si Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hao Zhou.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, H., Wang, CZ., Ye, JZ. et al. Solid-state fermentation of Ginkgo biloba L. residue for optimal production of cellulase, protease and the simultaneous detoxification of Ginkgo biloba L. residue using Candida tropicalis and Aspergillus oryzae . Eur Food Res Technol 240, 379–388 (2015). https://doi.org/10.1007/s00217-014-2337-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00217-014-2337-2

Keywords

Search

Navigation