Skip to main content
SpringerLink
Log in

Rhizopus oryzae as Fermentation Agent in Food Derived Sub-products

  • Original Paper
  • Published:
Waste and Biomass Valorization Aims and scope Submit manuscript

Abstract

The present research describes the use of Rhizopus oryzae as bioconversion agent of different agro-industrial by-products (fruit wastes, olive pulp cake, coffee grounds and potato peels) by solid state fermentation at different experimental conditions to enhance their value as animal feed. Results showed that R. oryzae grows better at fruit wastes than in other by-products. Fermentation process produced a protein and fat rich mycelia [respectively, 7.8 ± 1.2 and 9.0 ± 0.4% of dry matter (DM)] and reduced the carbohydrates content of considered by-products from 60.6 ± 0.4 to 40.1 ± 0.3% DM in 3 days. Supplementation with different nitrogen sources increases dramatically the protein concentration in the mycelia up to 46.8 ± 0.7% of DM. After fermentation, amino acid profile changed in the fermented product, with significant enrichment of several essential amino acids like valine, leucine, threonine, isoleucine and arginine and lower aspartate concentration. In conclusion, obtained product can be a high value alternative for 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

Similar content being viewed by others

References

  1. Stenmarck, Å., Jensen, C., Quested, T., Moates, G.: Estimates of European food waste levels. In: European Commission, Coordination and Support Action Stockholm, (2016)

  2. Villas-Boas, S.G., Esposito, E., Mitchell, D.A.: Microbial conversion of lignocellulosic residues for production of animal feeds. Anim. Feed Sci. Technol. 98(1–2), 1–12 (2002)

    Article  Google Scholar 

  3. Ugwuanyi, J.O., McNeil, B., Harvey, L.M.: Production of protein-enriched feed using agro-industrial residues as substrates. In: nee´Nigam, P.S., Pandey, A. (eds.) Biotechnology for Agro-Industrial Residues Utilisation, pp. 77–104. Springer, New York, (2009)

    Chapter  Google Scholar 

  4. Couto, S.R., Sanromán, M.Á.: Application of solid-state fermentation to food industry—a review. J. Food Eng. 76(3), 291–302 (2006)

    Article  Google Scholar 

  5. Budziszewska, J., Wilk, M., Wrzosek, M.: Taxonomic revision of the genus Rhizomucor. Paper presented at the IMC9: The Biology of Fungi, Edinburgh, UK

  6. Cantabrana, I., Perise, R., Hernández, I.: Uses of Rhizopus oryzae in the kitchen. Int. J. Gastron. Food Sci. 2(2), 103–111 (2015)

    Article  Google Scholar 

  7. Hachmeister, K.A., Fung, D.Y.C: Tempeh: a mold-modified indigenous fermented food made from soybeans and/or cereal grains. Crit. Rev. Microbiol. 19(3), 137–188 (1993)

    Article  Google Scholar 

  8. Lv, X.C., Huang, Z.Q., Zhang, W., Rao, P.F., Ni, L.: Identification and characterization of filamentous fungi isolated from fermentation starters for Hong Qu glutinous rice wine brewing. J. Gen. Appl. Microbiol. 58(1), 33–42 (2012)

    Article  Google Scholar 

  9. Ghosh, B., Ray, R.R.: Extra-cellular isoamylase production by Rhizopus oryzae in solid-state sermentation of agro wastes. Braz. Arch. Biol. Technol. 54(5), 867–876 (2011)

    Article  Google Scholar 

  10. Kim, H.-R., Kim, J.-H., Bai, D.-H., Ahn, B.-H.: Identification and characterization of useful fungi with alpha-amylase activity from the Korean traditional Nuruk. Mycobiology 39(4), 278–282 (2011)

    Article  Google Scholar 

  11. Bakir, U., Sebnem, Y., Ferda, G., Aysegul, E.: An endo-1,4-xylanase from Rhizopus oryzae: production, partial purification and biochemical characterization. Enzym. Microb. Technol. 29, 328–334 (2001)

    Article  Google Scholar 

  12. Benoit, I., Coutinho, P.M., Schols, H.A., Gerlach, J.P., Henrissat, B., de Vries, R.P.: Degradation of different pectins by fungi: correlations and contrasts between the pectinolytic enzyme sets identified in genomes and the growth on pectins of different origin. BMC Genomics 13, 321 (2012)

    Article  Google Scholar 

  13. Saito, K., Takakuwa, N., Oda, Y.: Purification of the extracellular pectinolytic enzyme from the fungus Rhizopus oryzae NBRC 4707. Microbiol. Res. 159(1), 83–86 (2004)

    Article  Google Scholar 

  14. Karmakar, M., Ray, R.R.: Extra celullar endoglucanase production by Rhizopus oryzae in solid and liquid state fermentation of agro wastes. Asian J. Biotechnol. 2, 27–36 (2010)

    Article  Google Scholar 

  15. Kupski, L., de Carvalho Silvello, M.A., Fontes, M.R.V., Lima, T.S., Treichel, H., Badiale Furlong, E.: R. oryzae cellulases: a new approach to degrading lignocellulosic material. J. Food Biochem. 39(2), 129–138 (2015)

    Article  Google Scholar 

  16. Liao, W., Liu, Y., Frear, C., Chen, S.: Co-production of fumaric acid and chitin from a nitrogen-rich lignocellulosic material—dairy manure—using a pelletized filamentous fungus Rhizopus oryzae ATCC 20344. Bioresour. Technol. 99(13), 5859–5866 (2008)

    Article  Google Scholar 

  17. Wang, G., Huang, D., Li, Y., Wen, J., Jia, X.: A metabolic-based approach to improve xylose utilization for fumaric acid production from acid pretreated wheat bran by Rhizopus oryzae. Bioresour. Technol. 180, 119–127 (2015)

    Article  Google Scholar 

  18. Xu, Q., Li, S., Fu, Y., Tai, C., Huang, H.: Two-stage utilization of corn straw by Rhizopus oryzae for fumaric acid production. Bioresour. Technol. 101(15), 6262–6264 (2010)

    Article  Google Scholar 

  19. Das, R.K., Brar, S.K., Verma, M.: A fermentative approach towards optimizing directed biosynthesis of fumaric acid by Rhizopus oryzae 1526 utilizing apple industry waste biomass. Fungal Biol. 119(12), 1279–1290 (2015)

    Article  Google Scholar 

  20. Gunawan-Puteri, M.D.P.T., Hassanein, T.R., Prabawati, E.K., Wijaya, C.H., Mutukumira, A.N.: Sensory characteristics of seasoning powders from overripe tempeh, a solid state fermented soybean. Procedia Chem. 14, 263–269 (2015)

    Article  Google Scholar 

  21. M’hir, S., Mejri, A., Sifaoui, I., Slama, M.B., Mejri, M., Thonart, P., Hamdi, M.: Improvement of protease production by Rhizopus oryzae CH4 grown on wheat. Arch. App. Sci. Res. 4(2), 1110–1116 (2012).

    Google Scholar 

  22. Lopez, E., Deive, F.J., Longo, M.A., Sanroman, M.A.: Strategies for utilisation of food-processing wastes to produce lipases in solid-state cultures of Rhizopus oryzae. Bioprocess Biosyst. Eng. 33(8), 929–935 (2010)

    Article  Google Scholar 

  23. Christen, P., Bramorski, A., Revah, S., Soccol, C.R.: Characterization of volatile compounds produced by Rhizopus strains grown on agro-industrial solid wastes. Bioresour. Technol. 71(3), 211–215 (2000)

    Article  Google Scholar 

  24. Hamdy, H.S.: Production of mini-food by Aspergillus niger, Rhizopus oryzae and Saccharomyces cerevisiae using orange peels. Rom. Biotech. Lett. 18(1), 7929–7946 (2013)

    Google Scholar 

  25. Oliveira, M.D.S., Feddern, V., Kupski, L., Cipolatti, E.P., Badiale-Furlong, E., de Souza-Soares, L.A.: Physico-chemical characterization of fermented rice bran biomass Caracterización fisico-química de la biomasa del salvado de arroz fermentado. CyTA J. Food 8(3), 229–236 (2010)

    Article  Google Scholar 

  26. Musa, R., Yunoki, K., Kinoshita, M., Oda, Y., Ohnishi, M.: Increased levels of policosanol and very long-chain fatty acids in potato pulp fermented with Rhizopus oryzae. Biosci. Biotechnol. Biochem. 68(11), 2401–2404 (2004)

    Article  Google Scholar 

  27. Massarolo, K.C., de Souza, T.D., Ribeiro, A.C., Furlong, E.B., de Souza Soares, L.A.: Influence of cultivation Rhizopus oryzae on rice bran on lipid fraction: fatty acids and phospholipids. Biocatal. Agric. Biotechnol. 8, 204–208 (2016)

    Google Scholar 

  28. Hackbart, H.C.S., Machado, A.R., Christ-Ribeiro, A., Prietto, L., Badiale-Furlong, E.: Reduction of aflatoxins by Rhizopus oryzae and Trichoderma reesei. Mycotoxin Res. 30(3), 141–149 (2014)

    Article  Google Scholar 

  29. Soccol, C.R., Iloki, I., Marin, B., Raimbault, M.: Comparative production of alpha-amylase, glucoamylase and protein enrichment of raw and cooked cassava by Rhizopus strains in submerged and solid-state fermentations. J. Food Sci. Technol. 31(4), 320–323 (1994)

    Google Scholar 

  30. Robinson, T., Nigam, P.: Bioreactor design for protein enrichment of agricultural residues by solid state fermentation. Biochem. Eng. J. 13(2–3), 197–203 (2003)

    Article  Google Scholar 

  31. Ferreira, J.A., Lennartsson, P.R., Niklasson, C., Lundin, M., Edebo, L., Taherzadeh, M.J.: Spent sulphite liquor for cultivation of an edible Rhizopus sp. BioResources 7(1), 173–188 (2012)

    Google Scholar 

  32. Calidad, C.d.I.y.C.d.l.: Análisis de alimentos: métodos oficiales y recomendados por el Centro de Investigación y Control de la Calidad. In: Consumo, M.d.S.y. (ed.). p. 1015. Ministerio de Sanidad y Consumo, (1985)

  33. Mamma, D., Topakas, E., Vafiadi, C., Christakopoulos, P.: Biotechnological potential of fruit processing industry residues. In: nee´Nigam, P.S., Pandey, A. (eds.) Biotechnology for Agro-Industrial Residues Utilisation, pp. 273–291. Springer, New York (2009)

    Chapter  Google Scholar 

  34. Vendruscolo, F., da Silva Ribeiro, C., Esposito, E., Ninow, J.L.: Protein enrichment of apple pomace and use in feed for Nile tilapia. Appl. Biochem. Biotechnol. 152(1), 74–87 (2009)

    Article  Google Scholar 

  35. Usaquen, S.M.: Aprovechamiento y valorización del alpeorujo tratado termicamente como: fertilizante biológco y fuente de hidroxitirosol Pontifia Universidad Javeriana (2008)

  36. Kupski, L., Cipolatti, E., da Rocha, M., Oliveira, M.D., Souza-Soares, L.D., Badiale-Furlong, E.: Solid-state fermentation for the enrichment and extraction of proteins and antioxidant compounds in rice bran by Rhizopus oryzae. Braz. Arch. Biol. Technol. 55(6), 937–942 (2012)

    Article  Google Scholar 

  37. Lennartsson, P.R., Taherzadeh, M.J., Edebo, L.: Rhizopus. In: Encyclopedia of food microbiology. Reference module in food safety, pp. 284–290. (2014).

    Chapter  Google Scholar 

  38. Huang, L.P., Jin, B., Lant, P., Zhou, J.: Simultaneous saccharification and fermentation of potato starch wastewater to lactic acid by Rhizopus oryzae and Rhizopus arrhizus. Biochem. Eng. J. 23(3), 265–276 (2005).

    Article  Google Scholar 

  39. Oboh, G., Elusiyan, C.A.: Changes in the nutrient and anti-nutrient content of micro-fungi fermented cassava flour produced from low- and medium-cyanide variety of cassava tubers. Afr. J. Biotechnol. 6(18), 2150–2157 (2007)

    Article  Google Scholar 

  40. Kayode, R.M.O., Sani, A.: Mineral compositions and amino acid profile of mono-culture fungal fermented mango (Mangifera Indica) kernel cake. J. Agric. Sci. 2(3), 69–74 (2010)

    Google Scholar 

  41. Yunoki, K., Musa, R., Kinoshita, M., Oda, Y., Ohnishi, M.: Determinations of triacylglycerol and fatty acid esters in potato pulp fermented with lactic acid-producing fungus. J. Oil Chem. Soc. Jpn. 53(11), 565–569 (2004)

    Google Scholar 

  42. Oliveira, M.D., Feddern, V., Kupski, L., Cipolatti, E.P., Badiale-Furlong, E., de Souza-Soares, L.A.: Changes in lipid, fatty acids and phospholipids composition of whole rice bran after solid-state fungal fermentation. Bioresour. Technol. 102(17), 8335–8338 (2011)

    Article  Google Scholar 

  43. Oda, Y., Yajima, Y., Kinoshita, M., Ohnishi, M.: Differences of Rhizopus oryzae strains in organic acid synthesis and fatty acid composition. Food Microbiol. 20(3), 371–375 (2003)

    Article  Google Scholar 

  44. Devrajan, A., Joshi, V.K., Gupta, K., Sheikher, C., Lal, B.B.: Evaluation of apple pomace based reconstituted feed in rats after solid state fermentation and ethanol recovery. Braz. Arch. Biol. Technol. 47(1), 93–106 (2004)

    Article  Google Scholar 

  45. Joshi, V.K., Sandhu, D.K.: Preparation and evaluation of an animal feed byproduct produced by solid-state fermentation of apple pomace. Bioresour. Technol. 56(2–3), 251–255 (1996)

    Article  Google Scholar 

  46. Upadhyaya, S., Tiwari, S., Arora, N., Singh, D.P.: Microbial protein: a valuable component for future food security. In: Singh, J.S., Singh, D.P. (eds.) Microbes and Environmental Management. Studium Press, New Delhi (2016)

    Google Scholar 

  47. FAO/WHO: Energy and Protein Requirements, pp. 1–118. WHO, Geneva (1973)

    Google Scholar 

  48. Wu, G., Bazer, F.W., Dai, Z., Li, D., Wang, J., Wu, Z.: Amino acid nutrition in animals: protein synthesis and beyond. Annu. Rev. Anim. Biosci. 2, 387–417 (2014)

    Article  Google Scholar 

  49. Verdú, J.M.: Tabla de composición de alimentos, 5 edn. Granada (2009)

Download references

Acknowledgements

Authors thank to Ainhoa Bikandi and Pilar Martín for their excellent technical support and to Sociedad Cooperativa “La Milagrosa” and Ekogras for providing the substrates. This work was funded by the Basque Government (Department of the Environment, Regional Planning, Agriculture and Fisheries).

Author information

Authors and Affiliations

  1. AZTI-Tecnalia, Food Research Division, Parque Tecnológico de Bizkaia, Astondo Bidea, Edf.609, 48160, Derio, Bizkaia, Spain

    Jone Ibarruri & Igor Hernández

Authors
  1. Jone Ibarruri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Igor Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Igor Hernández.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ibarruri, J., Hernández, I. Rhizopus oryzae as Fermentation Agent in Food Derived Sub-products. Waste Biomass Valor 9, 2107–2115 (2018). https://doi.org/10.1007/s12649-017-0017-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12649-017-0017-8

Keywords

Search

Navigation