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Solid State Fermentation of Brewer’s Spent Grain Using Rhizopus sp. to Enhance Nutritional Value

  • Jone IbarruriEmail author
  • Marta Cebrián
  • Igor Hernández
Original Paper
  • 39 Downloads

Abstract

In this study a valuable fermented brewer’s spent grain (BSG) was obtained by solid state fermentation (SSF) with Rhizopus sp. and assessed for feed and food applications. SSF conditions were optimized by factorial design and response surface methodology (RSM) to maximize the value of the resulting BSG biomass. Two Rhizopus sp. strains were tested as inoculum (one wild and one mutant strain) and time and temperature were analyzed. Measured response variables included, among others, protein content, soluble protein, degree of hydrolysis, antioxidant activity, total phenolic content and antibacterial activity. Both strains led to the highest protein concentration (31.7 ± 7.6%) and soluble protein (47.4 ± 3.8 mg/g DM) when BSG was fermented at 30 °C for 9 days. The biomass obtained presented a modified amino acid profile resulting in an essential amino acid index (EAAI) of 1.58 compared to FAO human nutrition standard, with antioxidant capacity (59.7 ± 7.7% DPPH reduction) and 11 times higher total polyphenol content (2.7 ± 0.1 mg GAE/g DM). Hereby, results demonstrate that SSF of BSG results in a significant increase of highly appreciated characteristics for feed or food applications, which could lead to a promising valorization alternative.

Keywords

Brewer’s spent grain Solid-state fermentation Rhizopus sp. Antioxidant capacity Protein enrichment 

Abbreviations

AA

Amino acids

EAA

Essential amino acids

EAAI

Essential amino acid index

FA

Fatty acids

DH

Degree of hydrolysis

TEAC

Trolox equivalent antioxidant capacity

DPPH

2,2-Diphenyl-1-picrylhydrazyl

TPC

Total phenolic content

Notes

Acknowledgements

Authors thank to Boga Cooperative for providing the BSG. This work was funded by the Basque Government (Department of Economic and Infrastructure Development, Agriculture, Fisheries and Food policy). This paper is Contribution No. 901 from AZTI (Food Research).

Funding

Funding was provided by Ekonomiaren Garapen eta Lehiakortasun Saila, Eusko Jaurlaritza.

Supplementary material

12649_2019_654_MOESM1_ESM.docx (2.8 mb)
Supplementary material 1 (DOCX 2847 KB)

References

  1. 1.
    Mussatto, S.I., Dragone, G., Roberto, I.C.: Brewers’ spent grain: generation, characteristics and potential applications. J. Cereal Sci. 43(1), 1–14 (2006).  https://doi.org/10.1016/j.jcs.2005.06.001 Google Scholar
  2. 2.
    Santos, M., Jiménez, J.J., Bartolomé, B., Gómez-Cordovés, C., del Nozal, M.J.: Variability of brewer’s spent grain within a brewery. Food Chem. 80(1), 17–21 (2003).  https://doi.org/10.1016/S0308-8146(02)00229-7 Google Scholar
  3. 3.
    Steiner, J., Procopio, S., Becker, T.: Brewer’s spent grain: source of value-added polysaccharides for the food industry in reference to the health claims. Eur. Food Res. Technol. 241(3), 303–315 (2015).  https://doi.org/10.1007/s00217-015-2461-7 Google Scholar
  4. 4.
    The Brewers of Europe.: Beer statistics 2017 edition. The Brewers of Europe, Bruxelles (2017)Google Scholar
  5. 5.
    Ikram, S., Huang, L.Y., Zhang, H.J., Wang, J., Yin, M.: Composition and nutrient value proposition of brewers spent grain. J. Food Sci. 82(10), 2232–2242 (2017).  https://doi.org/10.1111/1750-3841.13794 Google Scholar
  6. 6.
    McCarthy, A.L., O’Callaghan, Y.C., Piggott, C.O., FitzGerald, R.J., O’Brien, N.M.: Brewers’ spent grain; bioactivity of phenolic component, its role in animal nutrition and potential for incorporation in functional foods: a review. Proc. Nutr. Soc. 72(1), 117–125 (2013).  https://doi.org/10.1017/S0029665112002820 Google Scholar
  7. 7.
    Ozturk, S., Ozboy, O., Cavidoglu, I., Koksel, H.: Effects of brewer’s spent grain on the quality and dietary fibre content of cookies. J. Inst. Brew. 108(1), 23–27 (2002)Google Scholar
  8. 8.
    Weger, A., Jung, R., Stenzel, F., Hornung, A.: Optimized energetic usage of brewers’ spent grains. Chem. Eng. Technol. 40(2), 306–312 (2017).  https://doi.org/10.1002/ceat.201600186 Google Scholar
  9. 9.
    Russ, W., Mörtel, H., Meyer-Pittroff, R.: Application of spent grains to increase porosity in bricks. Constr. Build. Mater. 19(2), 117–126 (2005).  https://doi.org/10.1016/j.conbuildmat.2004.05.014 Google Scholar
  10. 10.
    Mishra, P.K., Gregor, T., Wimmer, R.: Utilising brewer’s spent grain as a source of cellulose nanofibres following separation of protein-based biomass. Bioresources. 12(1), 107–116 (2017).  https://doi.org/10.15376/biores.12.1.107-116 Google Scholar
  11. 11.
    Chiang, P.C., Chang, P., You, J.H.: Innovative technology fr controlling voc emissions. J. Hazard. Mater. 31(1), 19–28 (1992).  https://doi.org/10.1016/0304-3894(92)87036-f Google Scholar
  12. 12.
    Xiros, C., Christakopoulos, P.: Biotechnological potential of brewers spent grain and its recent applications. Waste Biomass Valoriz. 3(2), 213–232 (2012).  https://doi.org/10.1007/s12649-012-9108-8 Google Scholar
  13. 13.
    Carvalheiro, F., Esteves, M.P., Parajó, J.C., Pereira, H., Gírio, F.M.: Production of oligosaccharides by autohydrolysis of brewery’s spent grain. Bioresour. Technol. 91(1), 93–100 (2004).  https://doi.org/10.1016/S0960-8524(03)00148-2 Google Scholar
  14. 14.
    Almeida, A.D., Geraldo, M.R.F., Ribeiro, L.F., Silva, M.V., Maciel, M., Haminiuk, C.W.I.: Bioactive compounds from brewer’s spent grain: phenolic compounds, fatty acids and in vitro antioxidant capacity. Acta Sci.-Technol. 39(3), 269–277 (2017).  https://doi.org/10.4025/actascitechnol.v39i3.28435 Google Scholar
  15. 15.
    Connolly, A., O’Keeffe, M.B., Piggott, C.O., Nongonierma, A.B., FitzGerald, R.J.: Generation and identification of angiotensin converting enzyme (ACE) inhibitory peptides from a brewers’ spent grain protein isolate. Food Chem. 176, 64–71 (2015).  https://doi.org/10.1016/j.foodchem.2014.12.027 Google Scholar
  16. 16.
    Vieira, E., Teixeira, J., Ferreira, I.: Valorization of brewers’ spent grain and spent yeast through protein hydrolysates with antioxidant properties. Eur. Food Res. Technol. 242(11), 1975–1984 (2016).  https://doi.org/10.1007/s00217-016-2696-y Google Scholar
  17. 17.
    Radosavljevic, M., Pejin, J., Kocic-Tanackov, S., Mladenovic, D., Djukic-Vukovic, A., Mojovic, L.: Brewers’ spent grain and thin stillage as raw materials in l-(+)-lactic acid fermentation. J. Inst. Brew. 124(1), 23–30 (2018).  https://doi.org/10.1002/jib.462 Google Scholar
  18. 18.
    Gregori, A., Švagelj, M., Pahor, B., Berovič, M., Pohleven, F.: The use of spent brewery grains for Pleurotus ostreatus cultivation and enzyme production. N Biotechnol. 25(2), 157–161 (2008).  https://doi.org/10.1016/j.nbt.2008.08.003 Google Scholar
  19. 19.
    Sandhya, C., Sumantha, A., Szakacs, G., Pandey, A.: Comparative evaluation of neutral protease production by Aspergillus oryzae in submerged and solid-state fermentation. Process Biochem. 40(8), 2689–2694 (2005).  https://doi.org/10.1016/j.procbio.2004.12.001 Google Scholar
  20. 20.
    Nigam, P.S., Pandey, A.: Biotechnology for agro-industrial residues utilization. Springer, Dordrecht (2009)Google Scholar
  21. 21.
    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. Brazil. Arch. Biol. Technol. 55(6), 937–942 (2012).  https://doi.org/10.1590/S1516-89132012000600018 Google Scholar
  22. 22.
    Lizardi-Jimenez, M.A., Hernandez-Martinez, R.: Solid state fermentation (SSF): diversity of applications to valorize waste and biomass. 3 Biotech. 7(1), 44 (2017).  https://doi.org/10.1007/s13205-017-0692-y Google Scholar
  23. 23.
    Abd Razak, D.L., Abd Rashid, N.Y., Jamaluddin, A., Sharifudin, S.A., Abd Kahar, A., Long, K.: Cosmeceutical potentials and bioactive compounds of rice bran fermented with single and mix culture of Aspergillus oryzae and Rhizopus oryzae. J. Saudi Soc. Agric. Sci. 16(2), 127–134 (2017).  https://doi.org/10.1016/j.jssas.2015.04.001 Google Scholar
  24. 24.
    Cooray, S.T., Chen, W.N.: Valorization of brewer’s spent grain using fungi solid-state fermentation to enhance nutritional value. J. Funct. Foods. 42, 85–94 (2018).  https://doi.org/10.1016/j.jff.2017.12.027 Google Scholar
  25. 25.
    Ghosh, B., Ray, R.R.: Current commercial perspective of Rhizopus oryzae: a review. J. Appl. Sci. 11(14), 2470–2486 (2011).  https://doi.org/10.3923/jas.2011.2470.2486 Google Scholar
  26. 26.
    Meussen, B.J., de Graaff, L.H., Sanders, J.P., Weusthuis, R.A.: Metabolic engineering of Rhizopus oryzae for the production of platform chemicals. Appl. Microbiol. Biotechnol. 94(4), 875–886 (2012).  https://doi.org/10.1007/s00253-012-4033-0 Google Scholar
  27. 27.
    Cantabrana, I., Perise, R., Hernández, I.: Uses of Rhizopus oryzae in the kitchen. Int. J. Gastron. Food Sci. 2(2), 103–111 (2015).  https://doi.org/10.1016/j.ijgfs.2015.01.001 Google Scholar
  28. 28.
    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).  https://doi.org/10.1016/s0377-8401(02)00017-2 Google Scholar
  29. 29.
    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).  https://doi.org/10.1007/s00449-010-0416-8 Google Scholar
  30. 30.
    Hsiao, N.-W., Chen, Y., Kuan, Y.-C., Lee, Y.-C., Lee, S.-K., Chan, H.-H., Kao, C.-H.: Purification and characterization of an aspartic protease from the Rhizopus oryzae protease extract. Peptidase R. Electron. J. Biotechnol. 17(2), 89–94 (2014).  https://doi.org/10.1016/j.ejbt.2014.02.002 Google Scholar
  31. 31.
    Ibarruri, J., Hernández, I.: Rhizopus oryzae as fermentation agent in food derived sub-products. Waste Biomass Valoriz. 9(11), 2107–2115 (2018).  https://doi.org/10.1007/s12649-017-0017-8 Google Scholar
  32. 32.
    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
  33. 33.
    FazeliNejad, S., Ferreira, J.A., Brandberg, T., Lennartsson, P.R., Taherzadeh, M.J.: Fungal protein and ethanol from lignocelluloses using Rhizopus pellets under simultaneous saccharification, filtration and fermentation (SSFF). Biofuel Res. J. 3(1), 372–378 (2016).  https://doi.org/10.18331/brj2016.3.1.7 Google Scholar
  34. 34.
    Canedo, M.S., de Paula, F.G., da Silva, F.A., Vendruscolo, F.: Protein enrichment of brewery spent grain from Rhizopus oligosporus by solid-state fermentation. Bioprocess Biosyst. Eng. 39(7), 1105–1113 (2016).  https://doi.org/10.1007/s00449-016-1587-8 Google Scholar
  35. 35.
    Centro de Investigación y Control de la Calidad: Análisis de alimentos: métodos oficiales y recomendados por el Centro de Investigación y Control de la Calidad. Ministerio de Sanidad y Consumo, Madrid (1985)Google Scholar
  36. 36.
    UNE EN ISO.: Animal feeding stuffs—determination of amylase-treated neutral detergent fibre content (aNDF). (2006)Google Scholar
  37. 37.
    Satari, B., Karimi, K., Taherzadeh, M.J., Zamani, A.: Co-production of fungal biomass derived constituents and ethanol from citrus wastes free sugars without auxiliary nutrients in airlift bioreactor. Int. J. Mol. Sci. 17(3), 302 (2016).  https://doi.org/10.3390/ijms17030302 Google Scholar
  38. 38.
    Bligh, E.G., Dyer, W.J.: A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37(8), 911–917 (1959).  https://doi.org/10.1139/o59-099 Google Scholar
  39. 39.
    Waghmare, A.G., Salve, M.K., LeBlanc, J.G., Arya, S.S.: Concentration and characterization of microalgae proteins from Chlorella pyrenoidosa. Bioresour. Bioprocess. 3(1), 1 (2016).  https://doi.org/10.1186/s40643-016-0094-8 Google Scholar
  40. 40.
    FAO/WHO/UNU Expert Consultation. Protein and amino acid requirements in human nutrition, vol. 935. WHO Technical Report Series, Geneva (2007)Google Scholar
  41. 41.
    Nielsen, P.M., Petersen, D., Dambmann, C.: Improved method for determining food protein degree of hydrolysis. J. Food Sci. 66(5), 642–646 (2001).  https://doi.org/10.1111/j.1365-2621.2001.tb04614.x Google Scholar
  42. 42.
    Bougherra, F., Dilmi-Bouras, A., Balti, R., Przybylski, R., Adoui, F., Elhameur, H., Chevalier, M., Flahaut, C., Dhulster, P., Naima, N.: Antibacterial activity of new peptide from bovine casein hydrolyzed by a serine metalloprotease of Lactococcus lactis sub lattice BR16. J. Funct. Foods. 32(Supplement C), 112–122 (2017).  https://doi.org/10.1016/j.jff.2017.02.026 Google Scholar
  43. 43.
    Brand-Williams, W., Cuvelier, M.E., Berset, C.: Use of a free radical method to evaluate antioxidant activity. LWT—Food Sci. Technol. 28(1), 25–30 (1995).  https://doi.org/10.1016/S0023-6438(95)80008-5 Google Scholar
  44. 44.
    Singleton, V.L., Rossi, J.A.: Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 16(3), 144 (1965)Google Scholar
  45. 45.
    Miller, G.L.: Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31(3), 426–428 (1959).  https://doi.org/10.1021/ac60147a030 Google Scholar
  46. 46.
    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).  https://doi.org/10.1080/19476330903450274 Google Scholar
  47. 47.
    Rajesh, N., Imelda, J., Raj, R.P.: Value addition of vegetable wastes by solid-state fermentation using Aspergillus niger for use in aquafeed industry. Waste Manag. 30(11), 2223–2227 (2010).  https://doi.org/10.1016/j.wasman.2009.12.017 Google Scholar
  48. 48.
    Buenrostro-Figueroa, J.J., Velázquez, M., Flores-Ortega, O., Ascacio-Valdés, J.A., Huerta-Ochoa, S., Aguilar, C.N., Prado-Barragán, L.A.: Solid state fermentation of fig (Ficus carica L.) by-products using fungi to obtain phenolic compounds with antioxidant activity and qualitative evaluation of phenolics obtained. Process Biochem. 62, 16–23 (2017).  https://doi.org/10.1016/j.procbio.2017.07.016 Google Scholar
  49. 49.
    Ajila, C.M., Gassara, F., Brar, S.K., Verma, M., Tyagi, R.D., Valéro, J.R.: Polyphenolic antioxidant mobilization in apple pomace by different methods of solid-state fermentation and evaluation of its antioxidant activity. Food Bioprocess Technol. 5(7), 2697–2707 (2012).  https://doi.org/10.1007/s11947-011-0582-y Google Scholar
  50. 50.
    Fruet, A.P.B., Stefanello, F.S., Rosado Júnior, A.G., Souza, A.N.M.d., Tonetto, C.J., Nörnberg, J.L.: Whole grains in the finishing of culled ewes in pasture or feedlot: performance, carcass characteristics and meat quality. Meat Sci. 113, 97–103 (2016).  https://doi.org/10.1016/j.meatsci.2015.11.018 Google Scholar
  51. 51.
    Paraskevakis, N.: Effects of dietary dried Greek Oregano (Origanum vulgare ssp. hirtum) supplementation on blood and milk enzymatic antioxidant indices, on milk total antioxidant capacity and on productivity in goats. Anim. Feed Sci. Technol. 209, 90–97 (2015).  https://doi.org/10.1016/j.anifeedsci.2015.09.001 Google Scholar
  52. 52.
    Castillo, C., Pereira, V., Abuelo, A., Hernandez, J.: Effect of supplementation with antioxidants on the quality of bovine milk and meat production. Sci. World J. (2013)  https://doi.org/10.1155/2013/616098 Google Scholar
  53. 53.
    Wang, D., Sakoda, A., Suzuki, M.: Biological efficiency and nutritional value of Pleurotus ostreatus cultivated on spent beer grain. Bioresour. Technol. 78(3), 293–300 (2001).  https://doi.org/10.1016/S0960-8524(01)00002-5 Google Scholar
  54. 54.
    Dulf, F.V., Vodnar, D.C., Socaciu, C.: Effects of solid-state fermentation with two filamentous fungi on the total phenolic contents, flavonoids, antioxidant activities and lipid fractions of plum fruit (Prunus domestica L.) by-products. Food Chem. 209, 27–36 (2016).  https://doi.org/10.1016/j.foodchem.2016.04.016 Google Scholar
  55. 55.
    Correia, R.T.P., McCue, P., Magalhães, M.M.A., Macêdo, G.R., Shetty, K.: Production of phenolic antioxidants by the solid-state bioconversion of pineapple waste mixed with soy flour using Rhizopus oligosporus. Process Biochem. 39(12), 2167–2172 (2004).  https://doi.org/10.1016/j.procbio.2003.11.034 Google Scholar
  56. 56.
    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).  https://doi.org/10.1016/j.biortech.2011.06.025 Google Scholar
  57. 57.
    FEDNA. Fibra neutro detergente, Ácido detergente Y Lignina (FND,FAD,LAD secuenciales). http://fundacionfedna.org/tecnicas_de_analisis/fibra-neutro-detergente-%C3%A1cido-detergente-y-lignina-fndfadlad-secuenciales. Accessed 30 Sep, 2018
  58. 58.
    Ferret, A., Calsamiglia, S., Bach, A., Devant, M., Fernández, C., García-Rebollar, P.: Necesidades nutricionales para rumiantes de cebo. In: FEDNA (Fundación Española para el Desarrollo de la Nutrición Animal) (2008)Google Scholar
  59. 59.
    Kaur, V.: Incorporation of brewery waste in supplementary feed and its impact on growth in some carps. Bioresour. Technol. 91(1), 101–104 (2004).  https://doi.org/10.1016/s0960-8524(03)00073-7 MathSciNetGoogle Scholar
  60. 60.
    Miles, R.D., Chapman, F.A.: The benefits of fish meal in aquaculture diets. Institute of Food and Agricultural Sciences, University of Florida, Florida (2006)Google Scholar
  61. 61.
    Asadollahzadeh, M., Ghasemian, A., Saraeian, A., Resalati, H., Taherzadeh, M.: Production of fungal biomass protein by filamentous fungi cultivation on liquid waste streams from pulping process. BioResources. 13(1), 5013–5031 (2018).  https://doi.org/10.15376/biores.13.3.5013-5031 Google Scholar
  62. 62.
    Nitayavardhana, S., Issarapayup, K., Pavasant, P., Khanal, S.K.: Production of protein-rich fungal biomass in an airlift bioreactor using vinasse as substrate. Bioresour. Technol. 133, 301–306 (2013).  https://doi.org/10.1016/j.biortech.2013.01.073 Google Scholar
  63. 63.
    Wei, D., Li, M., Zhang, X., Ren, Y., Xing, L.: Identification and characterization of a novel delta12-fatty acid desaturase gene from Rhizopus arrhizus. FEBS Lett. 573(1–3), 45–50 (2004).  https://doi.org/10.1016/j.febslet.2004.06.100 Google Scholar
  64. 64.
    Innes, J.K., Calder, P.C.: Prostaglandins: Omega-6 fatty acids and inflammation. Leukot. Essent. Fatty Acids. 132, 41–48 (2018).  https://doi.org/10.1016/j.plefa.2018.03.004 Google Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Food Research DivisionAZTI. Parque Tecnológico de BizkaiaDerioSpain
  2. 2.Facultad de FarmaciaUniversidad del País Vasco/ Euskal Herriko UnibertsitateaVitoria-GasteizSpain

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