Abstract
Cassava bagasse is a by-product of the starch processing industry which contains a high quantity of starch and low protein content. Consequently, its application in animal feed is limited. In this study, solid-state fermentation was carried out to valorize this by-product. Two strains Aspergillus oryzae VS1 and Sporidiobolus pararoseus O1 were co-cultivated on cassava bagasse at 30 °C and 70% moisture to co-enrich protein, lipid, and β-carotene of cassava bagasse. Our result showed that at the inoculum size of log 9 cells of S. pararoseus O1 and log 6 spores of A. oryzae VS1 per gram of dry cassava bagasse, the protein, lipid, and β-carotene improved to 7.92%, 50.3 mg/g and 14.96 µg/g, respectively. Specially, the digestibility of organic matter increased 1.3-fold comparing to the initial cassava bagasse. To improve β-carotene content, several compounds were individually added to the solid-state fermentation namely ethanol, hydrogen peroxide, or citrate. The highest β-carotene accumulation of 48 µg/g dry cassava bagasse was attained using 1% citrate. Co-cultivation of A. oryzae and S. pararoseus using solid-state fermentation is a suitable approach to increase the nutritional value and β-carotene composition of cassava bagasse for animal feed application.
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The authors declare that all data supporting the findings of this study is available in this manuscript.
References
IMARC.: Cassava processing market: global industry trends, share, size, growth, opportunity and forecast 2021–2026 (2021)
Newby, J., Smith, D., Cramb, R., Delaquis, E., Yadav, L.: Cassava value chains and livelihoods in South-East-Asia, A regional research symposium held at Pematang Siantar North Sumatra, Indonesia, 1–5, July 2019. ACIAR proceedings Series, No. 148. Australia Center for International Agricultural Research (2020)
Pandey, A., Soccol, C.R., Nigam, P., Soccol, V.T., Vandenberghe, L.P.S., Mohan, R.: Biotechnological potential of agro-industrial residues. II: cassava bagasse. Bioresour Technol. 74, 81–87 (2000). https://doi.org/10.1016/S0960-8524(99)00143-1
John, R.P.: Biotechnological potentials of cassava bagasse. In: SinghNee Nigam, P., Pandey, A. (eds.) Biotechnology for Agro-industrial Residues Utilisation: Utilisation of Agro-residues, pp. 225–237. Springer, Dordrecht (2009)
Lounglawan, P., Khungaew, M., Suksombat, W.: Silage production from cassava peel and cassava pulp as energy source in cattle diets. J. Anim. Vet. Adv. 10, 1007–1011 (2011). https://doi.org/10.3923/javaa.2011.1007.1011
Green, A., Fascetti, A.: Meeting the vitamin A requirement: The efficacy and importance of β-carotene in animal species. Sci. World J. 2016, 1–22 (2016). https://doi.org/10.1155/2016/7393620
Cui, B., Liu, S., Wang, Q., Lin, X.: Effect of beta-carotene on immunity function and tumour growth in hepatocellular carcinoma rats. Molecules. 17, 8595–8603 (2012). https://doi.org/10.3390/molecules17078595
Jaswir, I., Noviendri, D., Hasrini, R., Octavianti, F.: Carotenoids: Sources, medicinal properties and their application in food and nutraceutical industry. J. Med. Plants Res. 5, 7119–7131 (2011). https://doi.org/10.5897/JMPRx11.011
Slaný, O., Klempová, T., Marcinčák, S., Čertík, M.: Production of high-value bioproducts enriched with γ-linolenic acid and β-carotene by filamentous fungi Umbelopsis isabellina using solid-state fermentations. Ann. Microbiol. 70, 5 (2020). https://doi.org/10.1186/s13213-020-01545-0
Mata-Gómez, L.C., Montañez, J.C., Méndez-Zavala, A., Aguilar, C.N.: Biotechnological production of carotenoids by yeasts: an overview. Microb. Cell. Fact. 13, 12 (2014). https://doi.org/10.1186/1475-2859-13-12
Roadjanakamolson, M., Suntornsuk, W.: Production of beta-carotene-enriched rice bran using solid-state fermentation of Rhodotorula glutinis. J. Microbiol. Biotechnol. 20, 525–531 (2010)
Abdelhafez, A.A., Husseiny, S.M., Abdel-Aziz Ali, A., Sanad, H.M.: Optimization of β-carotene production from agro-industrial by-products by Serratia marcescens ATCC 27117 using Plackett–Burman design and central composite design. Ann. Agric. Sci. 61, 87–96 (2016). https://doi.org/10.1016/j.aoas.2016.01.005
Lateef, A., Gueguim-Kana, E.B.: Utilization of cassava wastes in the production of fructosyltransferase by Rhizopus stolonifer LAU 07. Rom Biotechnol. Lett. 17, 7309–7316 (2012)
Adeoye, A.O., Lateef, A., Gueguim-Kana, E.B.: Optimization of citric acid production using a mutant strain of Aspergillus niger on cassava peel substrate. Biocatal. Agric. Biotechnol. 4, 568–574 (2015). https://doi.org/10.1016/j.bcab.2015.08.004
Lateef, A., Oloke, J., Kana, E., Oyeniyi, O., Onifade, O., Oyeleye, A., Oladosu, O., Oyelami, A.: Improving the quality of agro-wastes by solid-state fermentation: enhanced antioxidant activities and nutritional qualities. World J. Microbiol. Biotechnol. 24, 2369–2374 (2008). https://doi.org/10.1007/s11274-008-9749-8
Manan, M., Webb, C.: Design aspects of solid state fermentation as applied to microbial bioprocessing. J. Appl. Biotechnol. Bioeng. 4, 1–25 (2017). https://doi.org/10.15406/jabb.2017.04.00094
Soccol, C.R., Costa, E.S.F.d., Letti, L.A.J., Karp, S.G., Woiciechowski, A.L., Vandenberghe, L.P.d.S.: Recent developments and innovations in solid state fermentation. Biotechnol. Res. Innov. 1, 52–71 (2017). https://doi.org/10.1016/j.biori.2017.01.002
Martins, S., Mussatto, S.I., Martínez-Avila, G., Montañez-Saenz, J., Aguilar, C.N., Teixeira, J.A.: Bioactive phenolic compounds: Production and extraction by solid-state fermentation. A review. Biotechnol. Adv. 29, 365–373 (2011). https://doi.org/10.1016/j.biotechadv.2011.01.008
Lizardi-Jiménez, M.A., Hernández-Martínez, R.: Solid state fermentation (SSF): diversity of applications to valorize waste and biomass. 3 Biotech. 7, 44–44 (2017). https://doi.org/10.1007/s13205-017-0692-y
Cheng, Y., Liu, C., Cui, Y., Lv, T., Guo, Y., Liang, J., Qian, H.: Sporidiobolus pararoseus wall-broken powder ameliorates oxidative stress in diabetic nephropathy in type-2 diabetic mice by activating the Nrf2/ARE pathway. RSC Adv. 9, 8394–8403 (2019). https://doi.org/10.1039/C8RA10484K
Han, M., Xu, J.-Z., Liu, Z.-M., Qian, H., Zhang, W.-G.: Co-production of microbial oil and exopolysaccharide by the oleaginous yeast Sporidiobolus pararoseus grown in fed-batch culture. RSC Adv. 8, 3348–3356 (2018). https://doi.org/10.1039/C7RA12813D
Wang, H., Hu, B., Liu, J., Qian, H., Xu, J., Zhang, W.: Co-production of lipid, exopolysaccharide and single-cell protein by Sporidiobolus pararoseus under ammonia nitrogen-limited conditions. Bioprocess. Biosyst Eng. 43, 1403–1414 (2020). https://doi.org/10.1007/s00449-020-02335-3
Tapingkae, W., Panyachai, K., Yachai, M., Doan, H.V.: Effects of dietary red yeast (Sporidiobolus pararoseus) on production performance and egg quality of laying hens. J. Anim. Physiol. Anim. Nutr. 102, e337–e344 (2018). https://doi.org/10.1111/jpn.12751
Kot, A.M., Kieliszek, M., Piwowarek, K., Błażejak, S., Mussagy, C.U.: Sporobolomyces and Sporidiobolus – non-conventional yeasts for use in industries. Fungal Biol. Rev. 37, 41–58 (2021). https://doi.org/10.1016/j.fbr.2021.06.001
Hassan, M., Yang, Q., Xiao, Z.: Covalent immobilization of glucoamylase enzyme onto chemically activated surface of κ-carrageenan. Bull. Natl. Res. Cent. 43, e102 (2019). https://doi.org/10.1186/s42269-019-0148-0
Ghose, T.K.: Measurement of cellulase activities. Pure. Appl. Chem. 59, 257–268 (1987)
Michelon, M., de Matos de Borba, T., da Silva Rafael, R., Burkert, C.A.V., de Medeiros Burkert, J.F.: Extraction of carotenoids from Phaffia rhodozyma: A comparison between different techniques of cell disruption. Food Sci. Biotechnol. 21, 1–8 (2012). https://doi.org/10.1007/s10068-012-0001-9
López, J., Cataldo, V.F., Peña, M., Saa, P.A., Saitua, F., Ibaceta, M., Agosin, E.: Build your bioprocess on a solid strain—β-carotene production in recombinant Saccharomyces cerevisiae. Front. Bioeng. Biotechnol. (2019). https://doi.org/10.3389/fbioe.2019.00171
Folch, J., Lees, M., Stanley, S.: G.H.: A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497–509 (1957)
Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J.: Protein measurement with the folin phenol reagent. J. Biol. Chem. 193, 265–275 (1951)
AFIA.: Laboratory methods manual. A reference manual of standard methods for the analysis of fodder. Australia Fodder Industry Association LTD, Melbourne (2011)
Pham, T.A., Pham, K.N., To, K.A.: Efficient starch recovery from cassava bagasse: role of cellulase and pectinase. Vietnam J. Sci. Technol. 54, 401–409 (2019)
Han, M., He, Q., Zhang, W.G.: Carotenoids production in different culture conditions by Sporidiobolus pararoseus. Prep Biochem. Biotechnol. 42, 293–303 (2012). https://doi.org/10.1080/10826068.2011.583974
Chaiyaso, T., Manowattana, A.: Enhancement of carotenoids and lipids production by oleaginous red yeast Sporidiobolus pararoseus KM281507. Prep Biochem. Biotechnol. 48, 13–23 (2018). https://doi.org/10.1080/10826068.2017.1381620
Giani, M., Martínez-Espinosa, R.: Carotenoids as a protection mechanism against oxidative stress in Haloferax mediterranei. Antioxidants 9, 1060 (2020). https://doi.org/10.3390/antiox9111060
Sriherwanto, C.: Studies on the solid state fermentation of cassava bagasse for animal feed. Doctorate dissertation, University Hamburg, Germany (2010)
Garay, L.A., Sitepu, I.R., Cajka, T., Chandra, I., Shi, S., Lin, T., German, J.B., Fiehn, O., Boundy-Mills, K.L.: Eighteen new oleaginous yeast species. J. Ind. Microbiol. Biotechnol. 43, 887–900 (2016). https://doi.org/10.1007/s10295-016-1765-3
Krishna, C., Nokes, S.: Influence of inoculum size on phytase production and growth in solid-state fermentation by Aspergillus niger. Trans. ASAE 44, (2001). https://doi.org/10.13031/2013.6224
Abdullah, A.L., Tengerdy, R.P., Murphy, V.G.: Optimization of solid substrate fermentation of wheat straw. Biotechnol. Bioeng. 27, 20–27 (1985). https://doi.org/10.1002/bit.260270104
Lonsane, B.K., Saucedo-Castaneda, G., Raimbault, M., Roussos, S., Viniegra-Gonzalez, G., Ghildyal, N.P., Ramakrishna, M., Krishnaiah, M.M.: Scale-up strategies for solid state fermentation systems. Process. Biochem. 27, 259–273 (1992). https://doi.org/10.1016/0032-9592(92)85011-P
Al-Asheh, S., Duvnjak, Z.: Phytase production and decrease of phytic acid content in canola meal by Aspergillus carbonarius in solid-state fermentation. World J. Microbiol. Biotechnol. 11, 228–231 (1995). https://doi.org/10.1007/bf00704655
Yao, W., Nokes, S.E.: The use of co-culturing in solid substrate cultivation and possible solutions to scientific challenges. Biofuel Bioprod. Biorefin. 7, 361–372 (2013). https://doi.org/10.1002/bbb.1389
Raza, F., Raza, N.A., Hameed, U., Haq, I., Mariam, I.: Solid state fermentation for the production of beta-glucosidase by co-culture of Aspergillus niger and A. oryzae. Pak. J. Bot. 43, 75–83 (2011)
Aro, S.: Improvement in the nutritive quality of cassava and its by-products through microbial fermentation. Afr. J. Biotechnol. 725, 4789–4797 (2009)
Oboh, G.: Nutrient enrichment of cassava peels using a mixed culture of Saccharomyces cerevisae and Lactobacillus spp. solid media fermentation techniques. Electron. J. Biotechnol. (2006). https://doi.org/10.2225/vol9-issue1-fulltext-1
Yao, W., Nokes, S.: The use of co-culturing in solid substrate cultivation and possible solutions to scientific challenges. Biofuel Bioprod. Biorefin. (2013). https://doi.org/10.1002/bbb.1389
Pham, T.A., Hoang, T.N.T., Phung, T.T., To, K.A.: Factors enhancing the accumulation of beta-carotene in Rhodotorula taiwanensis CT1. Vietnam J. Sci. Technol. 58, 299–306 (2020)
Gu, W.L., An, G.H., Johnson, E.A.: Ethanol increases carotenoid production in Phaffia rhodozyma. J. Ind. Microbiol. Biotechnol. 19, 114–117 (1997). https://doi.org/10.1038/sj.jim.2900425
Marova, I., Breierová, E., Kočí, R., Friedl, Z., Slovak, B., Pokorna, J.: Influence of exogenous stress factors on production of carotenoids by some strains of cartenogenic yeasts. Ann. Microbiol. 54, 73–85 (2004)
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This study was supported by Vietnam’s Ministry of Education and Training (MOET), Grant No. B2019-BKA-05.
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Pham, T.A., Tran, L.N., Dam, T.H. et al. Valorization of Cassava Bagasse Using Co-culture of Aspergillus oryzae VS1 and Sporidiobolus pararoseus O1 in Solid-State Fermentation. Waste Biomass Valor 13, 3003–3012 (2022). https://doi.org/10.1007/s12649-022-01724-x
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DOI: https://doi.org/10.1007/s12649-022-01724-x