Skip to main content
SpringerLink
Log in

Immunomodulatory Properties of Filamentous Fungi Cultivated through Solid-State Fermentation on Rapeseed Meal

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

Abstract

Water extracts from solid-state fermentation (SSF) on rapeseed meal using filamentous fungi exhibit interesting immunomodulatory activities in vitro. Immunomodulation was determined by the capacity of the compounds to activate blood neutrophils and to influence cytokine production in human peripheral blood mononuclear cells (PBMC) and mouse bone marrow-derived macrophages (BMDM). Among the strains tested, Aspergillus sojae mycelium and SSF extracts were the most promising in terms of enhancing the immune response. The filamentous fungus was also successfully cultivated in a pre-pilot bioreactor with forced aeration. The results indicated that the extracts not only activated blood neutrophils but also significantly modulated IL-1β cytokine levels with lipopolysaccharide (LPS)-stimulated PBMC and BMDM without any cytotoxicity in immune cells. IL-1β was down-regulated in a dose-dependent manner in the presence of A. sojae crude mycelium and SSF extract with PBMC, which indicated that there was an anti-inflammatory activity, whereas IL-1β secretion was up-regulated in the presence of stimulated BMDM with the highest concentration that was tested (100 μg/mL). The non-fermented rapeseed had no effect at the same concentration. SSF culture, as a natural product, may be a good source for the development of functional feed with an immunostimulating effect or could potentially be used in medicinal applications.

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

Similar content being viewed by others

References

  1. OCDE/FAO. (2015). « Oléagineux et produits oléagineux », in Perspectives agricoles de l'OCDE et de la FAO 2015, Paris, Editions OCDE 2015.

  2. Ugwuanyi, J.O., McNeil, B. and Harvey, L.M. (2009). Production of protein-enriched feed using agro-industrial residues as substrates, in P. Singh-Nee Nigam, and A. Pandey (Eds.), Biotechnology for agro-industrial residues utilisation. Springer.77–103.

  3. Ramachandran, S., Singh, S. K., Larroche, C., Soccol, C. R., & Pandey, A. (2007). Oil cakes and their biotechnological applications—a review. Bioresource Technology, 98, 2000–2009.

    Article  CAS  Google Scholar 

  4. Wang, R., Shaarani, S. M., Godoy, L. C., Melikoglu, M., Vergara, C. S., Koutinas, A. A., & Webb, C. (2010). Bioconversion of rapeseed meal for the production of a generic microbial feedstock. Enzyme and Microbial Technology, 47, 77–83.

    Article  CAS  Google Scholar 

  5. Sivaramakrishnan, S. and Gangadharan, D. (2009). Edible oil cakes, in P. Singh-Nee Nigam, and A. Pandey (Eds.), Biotechnology for agro-industrial residues utilisation. Springer, 253–271.

  6. Holker, U., & Lenz, J. (2005). Solid-state fermentation—are there any biotechnological advantages? Current Opinion in Microbiology, 8, 301–306.

    Article  Google Scholar 

  7. Rodriguez Couto, S., & Sanroman, M. A. (2006). Application of solid-state fermentation to food industry—a review. Journal of Food Engineering, 76, 291–302.

    Article  Google Scholar 

  8. Pandey, A. (2003). Solid-state fermentation. Biochemical Engineering Journal, 13, 81–84.

    Article  CAS  Google Scholar 

  9. Villas-Boas, S. G., Esposito, E., & Mitchell, D. A. (2002). Microbial conversion of lignocellulosic residues for production of animal feeds. Animal Feed Science and Technology, 98, 1–12.

    Article  CAS  Google Scholar 

  10. Graminha, E. B. N., Gonçalves, A. Z. L., Pirota, R. D. P. B., Balsalobre, M. A. A., Da Silva, R., & Gomes, E. (2008). Enzyme production by solid-state fermentation: application to animal nutrition. Animal Feed Science and Technology, 144, 1–22.

    Article  CAS  Google Scholar 

  11. Bisaria, V. S., Saxena, S. K., Manihar, R. B., & Gopalkrishnan, K. S. (1984). Solid state fermentation of plant residues for improved animal feed by Pleurotus sp. Applied Biochemistry and Microbiology, 9, 341.

    Google Scholar 

  12. Kyanko, M. V., Canel, R. S., Ludemann, V., Pose, G., & Wagner, J. R. (2013). β-Glucan content and hydration properties of filamentous fungi. Applied Biochemistry and Microbiology, 49, 41–45.

    Article  CAS  Google Scholar 

  13. Lull, C., Wichers, H. J., & Savelkoul, H. F. (2005). Antiinflammatory and immunomodulating properties of fungal metabolites. Mediators of Inflammation, 2005, 63–80.

    Article  Google Scholar 

  14. Ramberg, J. E., Nelson, E. D., & Sinnott, R. A. (2010). Immunomodulatory dietary polysaccharides: a systematic review of the literature. Nutrition Journal, 9, 1–22.

    Article  Google Scholar 

  15. Jin, M., Jung, H. J., Choi, J. J., Jeon, H., Oh, J. H., Kim, B., Shin, S. S., Lee, J. K., Yoon, K. J., & Kim, S. (2003). Activation of selective transcription factors and cytokines by water-soluble extract from Lentinus lepideus. Experimental Biology and Medicine (Maywood), 228, 749–758.

    CAS  Google Scholar 

  16. Chan, G. C., Chan, W. K., & Sze, D. M. (2009). The effects of β-glucan on human immune and cancer cells. Journal of Hematology & Oncology, 2, 25.

    Article  Google Scholar 

  17. Volman, J. J., Ramakers, J. D., & Plat, J. (2008). Dietary modulation of immune function by β-glucans. Physiology and Behavior, 94, 276–284.

    Article  CAS  Google Scholar 

  18. El Enshasy, H. A., & Hatti-Kaul, R. (2013). Mushroom immunomodulators: unique molecules with unlimited applications. Trends in Biotechnology, 31, 668–677.

    Article  CAS  Google Scholar 

  19. Singh, R. S., Bhari, R., Rana, V., & Tiwary, A. K. (2011). Immunomodulatory and therapeutic potential of a mycelial lectin from Aspergillus nidulans. Applied Biochemistry and Microbiology, 165, 624–638.

    CAS  Google Scholar 

  20. Mahapatra, S., & Banerjee, D. (2013). Optimization of a bioactive exopolysaccharide production from endophytic Fusarium solani SD5. Carbohydrate Polymers, 97, 627–634.

    Article  CAS  Google Scholar 

  21. Takahashi, J.A. and Carvalho, S.A. (2010). Nutritional potential of biomass and metabolites from filamentous fungi, in A. Mendez-Vila (Ed.), Current research technology and education topics in applied microbiology and microbial biotechnology, Formatex, 1126–1135.

  22. Zuchowski, J., Pecio, L., Jaszek, M., & Stochmal, A. (2013). Solid-state fermentation of rapeseed meal with the white-rot fungi Trametes versicolor and Pleurotus ostreatus. Applied Biochemistry and Microbiology, 171, 2075–2081.

    CAS  Google Scholar 

  23. Shi, M., Yang, Y., Guan, D., Zhang, Y., & Zhang, Z. (2012). Bioactivity of the crude polysaccharides from fermented soybean curd residue by Flammulina velutipes. Carbohydrate Polymers, 89, 1268–1276.

    Article  CAS  Google Scholar 

  24. Svagelj, M., Berovic, M., Boh, B., Menard, A., Simcic, S., & Wraber, B. (2008). Solid-state cultivation of Grifola frondosa (dicks :Fr) S.F. Gray biomass and immunostimulatory effects of fungal intra- and extracellular β-polysaccharides. New Biotechnology, 25, 150–156.

    Article  CAS  Google Scholar 

  25. Kim, H., Suh, H. J., Kwon, K. H., Hwang, J. H., & Yu, K. W. (2016). Immunostimulation activity of a polysaccharide from fermented ginseng with Hericium erinaceum mycelia in solid-state culture. Food Science and Biotechnology, 25, 311–318.

    Article  CAS  Google Scholar 

  26. Nwe, N., Furuike, T., & Tamura, H. (2011). Production, properties and applications of fungal cell wall polysaccharides: chitosan and glucan. Advances in Polymer Science, 244, 187–208.

    Article  CAS  Google Scholar 

  27. Sugumaran, K. R., Jothi, P., & Ponnusami, V. (2014). Bioconversion of industrial solid waste—cassava bagasse for pullulan production in solid state fermentation. Carbohydrate Polymers, 99, 22–30.

    Article  CAS  Google Scholar 

  28. Yu, K. W., Kim, Y. S., Shin, K. S., Kim, J. M., & Suh, H. J. (2005). Macrophage-stimulating activity of exo-biopolymer from cultured rice bran with Monascus pilosus. Applied Biochemistry and Microbiology, 126, 35–48.

    CAS  Google Scholar 

  29. Li, S. (2014). Utilization of soybean curd residue for polysaccharides production by Morchella esculenta and evaluation of the biological activity. PhD thesis, University of Tsukuba, Japan.

  30. Durand, A. (2003). Bioreactor designs for solid state fermentation. Biochemical Engineering Journal, 13, 113–125.

    Article  CAS  Google Scholar 

  31. AOAC (1990). Official methods of analysis (15th ed.). Washington, DC., USA: Association of Official Analytical Chemists.

    Google Scholar 

  32. Maugé, L. (2013). Le modèle cellulaire THP-1: adaptation à l’étude de modulateurs de l’activité inflammatoire précoce implicant l’inflammasome. PhD thesis, Université de Bourgogne, France

  33. Roehm, N. W., Rodgers, G. H., Hatfield, S. M., & Glasebrook, A. L. (1991). An improved colorimetric assay for cell proliferation and viability utilizing the tetrazolium salt XTT. Journal of lmmunological Methods, 142, 257–265.

    Article  CAS  Google Scholar 

  34. Raimbault, M. (1998). General and microbiological aspects of solid substrate fermentation. Electronic Journal of Biotechnology, 1, 3.

    Article  Google Scholar 

  35. Smits, J. P., Rinzema, A., Tramper, J., Van Sonsbeek, H. M., Hage, J. C., Kaynak, A., & Knol, W. (1998). The influence of temperature on kinetics in solid-state fermentation. Enzyme Microbial Technology, 22, 50–57.

    Article  CAS  Google Scholar 

  36. Roussos, S., Hannibal, L., Durand, A., Diez, M., Saucedo, G., & Montet, D. (1994). Protein enrichment of copra cake—selection of filamentous fungi in SSF. Oléagineux, 49, 235–247.

    CAS  Google Scholar 

  37. Terebiznik, M. R., & Pilosof, A. M. R. (1999). Biomass estimation in solid state fermentation by modeling dry matter weight loss. Biotechnology Techniques, 13, 215–219.

    Article  CAS  Google Scholar 

  38. Farinas, C. S., Vitcosque, G. L., Fonseca, R. F., Neto, V. B., & Couri, S. (2011). Modeling the effects of solid state fermentation operating conditions on endoglucanase production using an instrumented bioreactor. Industrial Crops and Products, 34, 1186–1192.

    Article  CAS  Google Scholar 

  39. Lee, Y. T., & Kim, Y. S. (2005). Water-solubility of β-glucans in various edible mushrooms. Journal of Food Science and Nutrition, 10, 294–297.

    CAS  Google Scholar 

  40. Martins, S., Mussatto, S. I., Martinez-Avila, G., Montanez-Saenz, J., Aguilar, C. N., & Teixeira, J. A. (2011). Bioactive phenolic compounds: production and extraction by solid-state fermentation. A review. Biotechnology Advances, 29, 365–373.

    Article  CAS  Google Scholar 

  41. Daniel, P. S., Abba, I. T., & Tristram, G. P. (1994). Basic and clinical immunology (8th ed.pp. 195–215). USA: Appleton and Lange.

    Google Scholar 

  42. Castro, R., Couso, N., Obach, A., & Lamasa, J. (1999). Effect of different β-glucans on the respiratory burst of turbot (Psetta maxima) and gilthead seabream (Sparus aurata) phagocytes. Fish & Shellfish Immunology, 9, 529–541.

    Article  CAS  Google Scholar 

  43. Jang, S. A., Kang, S. C., & Sohn, E. H. (2011). Phagocytic effects of β-glucans from the mushroom Coriolus versicolor are related to dectin-1, NOS, TNF-α signaling in macrophages. Biomolecules and Therapeutics, 19, 438–444.

    Article  CAS  Google Scholar 

  44. Chen, J., & Seviour, R. (2007). Medicinal importance of fungal b-(1/3), (1/6)-glucans. Mycological Research, 111, 635–652.

    Article  CAS  Google Scholar 

  45. Dinarello, C. A. (1994). The biological properties of interleukin-1. European Cytokine Network, 5, 517–531.

    CAS  Google Scholar 

  46. Poutsiaka, D. D., Mengozzi, M., Vannier, E., Sinha, B., & Dinarello, C. A. (1993). Cross-linking of the beta-glucan receptor on human monocytes results in interleukin-1 receptor antagonist but not interleukin-1 production. Blood, 82, 3695–3700.

    CAS  Google Scholar 

  47. Luhm, J., Langenkamp, U., Hensel, J., Frohn, C., Brand, J. M., Hennig, H., Rink, L., Koritke, P., Wittkopf, N., Williams, D. L., & Mueller, A. (2012). β-(1 → 3)-D-glucan modulates DNA binding of nuclear factors κB, AT and IL-6 leading to an anti-inflammatory shift of the IL-1β/IL-1 receptor antagonist ratio. BMC Immunology, 2006, 7–5.

    Google Scholar 

  48. Smeekens, S. P., Gresnigt, M. S., Becker, K. L., Cheng, S. C., Netea, S. A., Jacobs, L., Jansen, T., Veerdonk, F. L., Williams, D. L., Joosten, L. A. B., Dinarello, C. A., & Netea, M. G. (2015). An anti-inflammatory property of Candida albicans β-glucan: induction of high levels of interleukin-1 receptor antagonist via a dectin-1/CR3 independent mechanism. Cytokine, 71, 215–222.

    Article  CAS  Google Scholar 

  49. Ji, Z., Tang, Q., Zhang, J., Yang, Y., Jia, W., & Pan, Y. (2007). Immunomodulation of RAW264.7 macrophages by GLIS, a proteopolysaccharide from Ganoderma lucidum. Journal of Ethnopharmacology, 112, 445–450.

    Article  CAS  Google Scholar 

  50. Lin, Z. B. (2005). Cellular and molecular mechanisms of immuno-modulation by Ganoderma lucidum. Journal of Pharmacological Sciences, 99, 144–153.

    Article  CAS  Google Scholar 

  51. Hsu, H. Y., Hua, K. F., Lin, C. C., Lin, C. H., Hsu, J., & Wong, C. H. (2004). Extract of Reishi polysaccharides induces cytokine expression via TLR4-modulated protein kinase signaling pathways. The Journal of Immunology, 173, 5989–5999.

    Article  CAS  Google Scholar 

  52. Suzuki, I., Tanaka, H., Kinoshita, A., Oikawa, S., Osawa, M., & Yadomae, T. (1990). Effect of orally administered β-glucan on macrophage function in mice. International Journal of Immunopharmacology, 12, 675–684.

    Article  CAS  Google Scholar 

  53. Municio, C., Alvarez, Y., Montero, O., Hugo, E., Rodriguez, M., Domingo, E., Alonso, S., Fernandez, N., & Crespo, M. S. (2013). The response of human macrophages to β-glucans depends on the inflammatory milieu. PloS One, 8, e62016.

    Article  CAS  Google Scholar 

  54. Thevenieau, F., Bourdillon, A., Durand, A., De Coninck, J. and Sutter, S. (2015). Produit alimentaire et son procédé d'obtention. Fidop. Patent WO 2015101650 A3, 27/08/2015.

Download references

Acknowledgements

The authors would like to thank the Fonds De Developpement Des Filieres Des Oleagineux Et Des Proteagineux for funding this research. We are grateful to Dr. S. Delemasure-Chalumeau and Dr. P. Dutartre (Cohiro Biotechnology) for their contributions to the immune assay and statistical analysis.

Author information

Authors and Affiliations

  1. Welience, Plateforme de Prédéveloppement en Biotechnologies, site INRA, 17 rue de Sully, 21000, Dijon, France

    Stéphanie Sutter & Joëlle De Coninck

  2. University Bourgogne Franche-Comté, AgroSup Dijon, PAM UMR A 02.102, F-21000, Dijon, France

    Stéphanie Sutter & Joëlle De Coninck

  3. Groupe Avril-Direction Innovation, 11 Rue de Monceau, 75378, Paris, Cedex 08, France

    France Thevenieau & Anne Bourdillon

Authors
  1. Stéphanie Sutter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. France Thevenieau
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anne Bourdillon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joëlle De Coninck
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stéphanie Sutter.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sutter, S., Thevenieau, F., Bourdillon, A. et al. Immunomodulatory Properties of Filamentous Fungi Cultivated through Solid-State Fermentation on Rapeseed Meal. Appl Biochem Biotechnol 182, 910–924 (2017). https://doi.org/10.1007/s12010-016-2370-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-016-2370-7

Keywords

Search

Navigation