Bacillus cereus-mediated biofermentation of Sardine offal waste: A novel approach to enhance nutritional value by Response Surface Methodology optimization
Article Main
Abstract
The rising protein demand in the aquaculture sector has significantly impacted fishmeal supply and pricing. Excessive use of fishmeal can lead to environmental issues and negatively impact marine biodiversity and human food security. Consequently, finding alternative fishmeal in aquaculture is crucial for economic and environmental sustainability. The present study aimed to determine how Bacillus cereus (MT355408) could enhance nutritional value of Sardine fish waste, which could replace fish meal in the market. Solid-state fermentation (SSF) represents a biotechnological method that utilizes microbes to convert discarded fish byproducts into valuable products. The bacterial ability to produce enzymes was studied and optimised for its maximum production to be used as an inoculum for the SSF technique. Different prebiotic sources were also studied for better upliftment of bacteria in the solid-state surface. A single-factor analysis was conducted to investigate the influence of varying prebiotic concentrations, inoculum quantity, and fermentation duration on protein breakdown. After studying the single-factor tests, a further response surface model was employed for better yield. The results indicated that the highest protein yield could be achieved with a fermentation time of 132.893 hours, a prebiotic quantity of 25%, and an inoculum quantity of 5.3%. The study's findings also affirmed that the model was vital in enhancing the crude protein content during fermentation. In conclusion, the model's results contribute valuable insights into fermentation processes, offering practical implications for enhancing protein content and digestibility in similar contexts.
Article Details
Article Details
Keywords
Bacteria, Fish waste, Prebiotics, Response surface methodology, Solid state fermentation
References
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Alahmad, Aljammas, H., Yazji, S. & Azizieh, A. (2022). Optimization of protease production from Rhizomucor miehei Rm4 isolate under solid-state fermentation. Journal of Genetic Engineering and Biotechnology, 20(1),1-3. https://doi.org/10.1186/s43141-022-00358-9.
Araujo, J., Sica, P., Costa, C. & Márquez, M.C. (2021). Enzymatic hydrolysis of fish waste as an alternative to produce high value-added products. Waste and Biomass Valorization, 12, 847-55. https://doi.org/10.1007/s12649-020-01029-x.
Asha, B. & Palaniswamy, M. (2018). Optimization of alkaline protease production by Bacillus cereus FT 1isolated from soil. Journal of Applied Pharmaceutical Science, 8(2), 119-27. 10.7324/JAPS.2018.8219.
Briki, S., Hamdi, O. & Landoulsi, A. (2016). Enzymatic dehairing of goat skins using alkaline protease from Bacillus sp. SB12. Protein Expression and Purification, 121, 9–16. 10.1016/j.pep.2015.12.021.
Cahyaningtyas, H. A., Suyotha, W., Cheirsilp, B. & Yano, S. (2021). Statistical optimization of halophilic chitosanase and protease production by Bacillus cereus HMRSC30 isolated from Terasi simultaneous with chitin extraction from shrimp shell waste. Biocatalysis and Agricultural Biotechnology, 1, 31:101918. https://doi.org/10.1016/j.bcab.2021.101918.
Cupp -enyard, C. (2008). Sigma’s Non-specific Protease Activity Assay - Casein as a Substrate. Journal of visualized experiments, 10,3791/899.
Do Nascimento, R. P., Junior, N. A. & Coelho, R. R. R. (2011). Brewer’s spent grain and corn steep liquor as alternative culture medium substrates for proteinase production by Streptomyces malaysiensis AMT-3. Brazilian Journal of Microbiology, 42(4), 1384–1389. 10.1590/S1517-838220110004000020.
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Islam, F. & Roy, N. (2018). Screening, purification and characterization of cellulase from cellulase producing bacteria in molasses. BMC Research Notes, 11(1), 445. https://doi.org/10.1186/s13104-018-3558-4.
Imran, S.Z. & Wei, L.S. (2019). Selected Essential Amino Acid Enhancement by Bacillus cereus from Solid State Fermentation of Soy Pulp Through Carbon Concentration and Fermentation Period. Journal of Aquaculture Research & Development, 10(566), p.2. 10.4172/2155-9546.1000566.
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Kamizake, N.K., Gonçalves, M.M., Zaia, C.T. & Zaia, D.A. (2003). Determination of total proteins in cow milk powder samples: a comparative study between the Kjeldahl method and spectrophotometric methods. Journal of Food composition and analysis, 16(4),507-516. https://doi.org/10.1016/S0889-1575(03)00004-8.
Lee, L. P., Karbul, H. M., Citartan, M., Gopinath, S. C. B., Lakshmipriya, T. & Tang, T. H. (2015). Lipase-Secreting Bacillus Species in an Oil-Contaminated Habitat: Promising Strains to Alleviate Oil Pollution. BioMed Research International, 820575. https://doi.org/10.1155/2015/820575.
Luang-In, V., Yotchaisarn, M., Saengha, W., Udomwong, P., Deeseenthum, S. M. & Maneewan, K. (2019). Isolation and Identification of Amylase-producing Bacteria from Soil in Nasinuan Community Forest, Maha Sarakham, Thailand. Biomedical and Pharmacology Journal, 12(3), 1061–1068. https://dx.doi.org/10.13005/bpj/1735.
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López-Trujillo, J., Mellado-Bosque, M., Ascacio-Valdés, J. A., Prado-Barragán, L. A., Hernández-Herrera, J. A. & Aguilera-Carbó, A. F. (2023). Temperature and pH Optimization for Protease Production Fermented by Yarrowia lipolytica from Agro-Industrial Waste. Fermentation, 9(9), 819. https://doi.org/10.3390/fermentation9090819.
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Masi, C., Gemechu, G. & Tafesse, M. (2021). Isolation, screening, characterization, and identification of alkaline protease-producing bacteria from leather industry effluent. Annals of Microbiology, 71(1), 1–11. https://doi.org/10.1186/s13213-021-01631-x.
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Molinuevo-Salces, B., Ahring, B.K. &Uellendahl, H. (2015). Optimization of the co-digestion of catch crops with manure using a central composite design and reactor operation. Applied biochemistry and biotechnology, 175,1710-1723. 10.1007/s12010-014-1391-3.
Nkhata, S. G., Ayua, E., Kamau, E. H. & Shingiro, J. B. (2018). Fermentation and germination improve nutritional value of cereals and legumes through activation of endogenous enzymes. Food Science & Nutrition, 6(8), 2446–2458. https://doi.org/10.1002/fsn3.846.
Nielsen, P. M., Petersen, D. & Dambmann, C. (2001). Improved Method for Determining Food Protein Degree of Hydrolysis. Food chemistry and toxicology 66:5. https://doi.org/10.1111/j.1365-2621.2001.tb04614.x
Oreopoulou, V. & Russ, W. (2006). Utilization of Byproducts and Treatment of Waste in the Food Industry. Springer Science & Business Media.
Patsios, S. I., Dedousi, A., Sossidou, E. Ν. & Zdragas, A. (2020). Sustainable Animal Feed Protein through the Cultivation of YARROWIA Lipolytica on Agro-Industrial Wastes and byproducts. Sustainability: Science Practice and Policy, 12(4), 1398. https://doi.org/10.3390/su12041398.
Ravindran, B., Wong, J. W. C., Selvam, A., Thirunavukarasu, K. & Sekaran, G. (2016). Microbial biodegradation of proteinaceous tannery solid waste and production of a novel value-added product - Metalloprotease. Bioresource Technology, 217, 150–156. 10.1016/j.biortech.2016.03.033.
Samuel, R.A., Dash, S.S., Ali, L. Riyas. & Paari, K.A. (2021). Formulation and characterization of plant, animal, and probiotic based fish meals and evaluating their efficacy on growth and performance in zebrafish (danio rerio). Advances in Animal and Veterinary Sciences, 9(8)
Silva, J.F.X., Ribeiro, K., Silva, J.F., Cahú, T.B. & Bezerra, R.S. (2014). Utilization of tilapia processing waste for the production of fish protein hydrolysate. Animal feed science and technology, 196, 96-106. https://doi.org/10.1016/j.anifeedsci.2014.06.010
Simat, V. (2021). Valorization of seafood processing byproducts. In Valorization of agri-food wastes and byproducts. Agricultural and biological sciences, 515-536.
Shyam, S.S. & Akhila, K. (2022). Domestic fish consumption in India: Challenges and opportunities, Shrimp farming – made better for the Future ,10-25.
Solanki, P., Putatunda, C., Kumar, A., Bhatia, R. & Walia, A. (2021). Microbial proteases: ubiquitous enzymes with innumerable uses. 3 Biotech, 11(10), 428. https://doi.org/10.1007/s13205-021-02928-z.
Tropea, A., Potortì, A. G., Lo Turco, V., Russo, E., Vadalà, R., Rando, R. & Di Bella, G. (2021). Aquafeed Production from Fermented Fish Waste and Lemon Peel. Fermentation, 7(4), 272. https://doi.org/10.3390/fermentation7040272.
Tennalli, G.B., Garawadmath, S., Sequeira, L., Murudi, S., Patil, V., Divate, M.N.& Hungund, B.S. (2022). Media optimization for the production of alkaline protease by Bacillus cereus PW3A using response surface methodology. Journal of Applied Biology and Biotechnology, 1,10(4)-17-26.
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Abidin, Z., Huang, H.T., Hu, Y.F., Chang, J.J., Huang, C.Y., Wu, Y.S. & Nan, F.H. (2022). Effect of dietary supplementation with Moringa oleifera leaf extract and Lactobacillus acidophilus on growth performance, intestinal microbiota, immune response, and disease resistance in whiteleg shrimp (Penaeus vannamei). Fish & Shellfish Immunology, 127, 876-890. https://doi.org/10.1016/j.fsi.2022.07.007.
Afreen, M. & Ucak, I. (2020). Fish processing wastes used as feed ingredient for animal feed and aquaculture feed. Journal of Survey in Fisheries Sciences, 55-64. https://doi.org/10.17762/sfs.v6i2.198
Alahmad, Aljammas, H., Yazji, S. & Azizieh, A. (2022). Optimization of protease production from Rhizomucor miehei Rm4 isolate under solid-state fermentation. Journal of Genetic Engineering and Biotechnology, 20(1),1-3. https://doi.org/10.1186/s43141-022-00358-9.
Araujo, J., Sica, P., Costa, C. & Márquez, M.C. (2021). Enzymatic hydrolysis of fish waste as an alternative to produce high value-added products. Waste and Biomass Valorization, 12, 847-55. https://doi.org/10.1007/s12649-020-01029-x.
Asha, B. & Palaniswamy, M. (2018). Optimization of alkaline protease production by Bacillus cereus FT 1isolated from soil. Journal of Applied Pharmaceutical Science, 8(2), 119-27. 10.7324/JAPS.2018.8219.
Briki, S., Hamdi, O. & Landoulsi, A. (2016). Enzymatic dehairing of goat skins using alkaline protease from Bacillus sp. SB12. Protein Expression and Purification, 121, 9–16. 10.1016/j.pep.2015.12.021.
Cahyaningtyas, H. A., Suyotha, W., Cheirsilp, B. & Yano, S. (2021). Statistical optimization of halophilic chitosanase and protease production by Bacillus cereus HMRSC30 isolated from Terasi simultaneous with chitin extraction from shrimp shell waste. Biocatalysis and Agricultural Biotechnology, 1, 31:101918. https://doi.org/10.1016/j.bcab.2021.101918.
Cupp -enyard, C. (2008). Sigma’s Non-specific Protease Activity Assay - Casein as a Substrate. Journal of visualized experiments, 10,3791/899.
Do Nascimento, R. P., Junior, N. A. & Coelho, R. R. R. (2011). Brewer’s spent grain and corn steep liquor as alternative culture medium substrates for proteinase production by Streptomyces malaysiensis AMT-3. Brazilian Journal of Microbiology, 42(4), 1384–1389. 10.1590/S1517-838220110004000020.
Essabiri, H., Damrani, R., Boumalkha, O., Hachi, T., Laiboud, C. & Abba, E.H. (2022). Fish waste: Valorisation methods on a local scale. InIOP Conference Series: Earth and Environmental Science , 1090(1)- 012015. 10.1088/1755-1315/1090/1/012015.
Gaddad, S.M. (2019). Enhanced production of extracellular alkaline protease by Bacillus cereus GVK21 by optimized formulations. International Journal of Pharmacy and Biological Sciences, Transactions B: Applications, 9(1),1103-13.
Hadjidj, R., Badis, A., Mechri, S., Eddouaouda, K., Khelouia, L., Annane, R., El, Hattab. M. & Jaouadi, B. (2018). Purification, biochemical, and molecular characterization of novel protease from Bacillus licheniformis strain K7A. International Journal of Biological Macromolecules,114,1033-48. https://doi.org/10.1016/j.ijbiomac.201 8.03.167.
Hammoumi, A., Faid, M. & Amarouch, H. (1998). Characterization of fermented fish waste used in feeding trials with broilers. Process Biochemistry, 33(4), 423-427. https://doi.org/10.1016/S0032-9592(97)00092-7.
Harun, A.A.C., Mohammad, N.A.H., Ikhwanuddin, M., Jauhari, I., Sohaili, J. & Kasan, N.A. (2019). Effect of different aeration units, nitrogen types and inoculum on biofloc formation for improvement of Pacific Whiteleg shrimp production. The Egyptian Journal of Aquatic Research, 45(3), 287-292. https://doi.org/10.1016/j.ejar.2019.07.001
Hashmi, S., Iqbal, S., Ahmed, I. & Janjua, H.A., (2022). Production, optimization, and partial purification of alkali-thermotolerant proteases from newly isolated Bacillus subtilis S1 and Bacillus amyloliquefaciens KSM12. Processes, 10(6),1050. https://doi.org/10.3390/pr10061050.
Islam, F. & Roy, N. (2018). Screening, purification and characterization of cellulase from cellulase producing bacteria in molasses. BMC Research Notes, 11(1), 445. https://doi.org/10.1186/s13104-018-3558-4.
Imran, S.Z. & Wei, L.S. (2019). Selected Essential Amino Acid Enhancement by Bacillus cereus from Solid State Fermentation of Soy Pulp Through Carbon Concentration and Fermentation Period. Journal of Aquaculture Research & Development, 10(566), p.2. 10.4172/2155-9546.1000566.
Kieliszek, M., Pobiega, K., Piwowarek, K. & Kot, A. M. (2021). Characteristics of the Proteolytic Enzymes Produced by Lactic Acid Bacteria. Molecules, 26(7). https://doi.org/10.3390/molecules26071858.
Kamizake, N.K., Gonçalves, M.M., Zaia, C.T. & Zaia, D.A. (2003). Determination of total proteins in cow milk powder samples: a comparative study between the Kjeldahl method and spectrophotometric methods. Journal of Food composition and analysis, 16(4),507-516. https://doi.org/10.1016/S0889-1575(03)00004-8.
Lee, L. P., Karbul, H. M., Citartan, M., Gopinath, S. C. B., Lakshmipriya, T. & Tang, T. H. (2015). Lipase-Secreting Bacillus Species in an Oil-Contaminated Habitat: Promising Strains to Alleviate Oil Pollution. BioMed Research International, 820575. https://doi.org/10.1155/2015/820575.
Luang-In, V., Yotchaisarn, M., Saengha, W., Udomwong, P., Deeseenthum, S. M. & Maneewan, K. (2019). Isolation and Identification of Amylase-producing Bacteria from Soil in Nasinuan Community Forest, Maha Sarakham, Thailand. Biomedical and Pharmacology Journal, 12(3), 1061–1068. https://dx.doi.org/10.13005/bpj/1735.
Li, C., Ma, L., Wang, L., Zhang, Z., Chen, Y., Chen, J., Jiang, Q., Song, Z., He, X., Tan, B., Xiao, D. & Ma, X. (2023). Optimization of Solid-State Fermentation Conditions of Quercus liaotungensis by Bacillus subtilis. Fermentation, 9(1), 75. https://doi.org/10.3390/fermentation9010075.
López-Trujillo, J., Mellado-Bosque, M., Ascacio-Valdés, J. A., Prado-Barragán, L. A., Hernández-Herrera, J. A. & Aguilera-Carbó, A. F. (2023). Temperature and pH Optimization for Protease Production Fermented by Yarrowia lipolytica from Agro-Industrial Waste. Fermentation, 9(9), 819. https://doi.org/10.3390/fermentation9090819.
Manfredini, P.G., Cavanhi, V.A., Costa, J.A. & Colla, L. M. (2021). Bioactive peptides and proteases: characteristics, applications and the simultaneous production in solid-state fermentation. Biocatalysis and Biotransformation, 39(5),360-77. https://doi.org/10.1080/ 10242422. 2020. 1849 151.
Masi, C., Gemechu, G. & Tafesse, M. (2021). Isolation, screening, characterization, and identification of alkaline protease-producing bacteria from leather industry effluent. Annals of Microbiology, 71(1), 1–11. https://doi.org/10.1186/s13213-021-01631-x.
Mathew, G. M., Huang, C. C., Sindhu, R., Binod, P., Sirohi, R., Awsathi, M. K., Pillai, S. & Pandey, A. (2021). Enzymatic approaches in the bioprocessing of shellfish wastes. Biotech, 11(8), 367.
Mayta-Apaza, A.C., García-Cano, I., Dabrowski, K. & Jiménez-Flores, R. (2021). Bacterial diversity analysis and evaluation proteins hydrolysis during the acid whey and fish waste fermentation. Microorganisms, 9(1),100. https://doi.org/10.3390/microorganisms9010100.
Mcbride, C. H. (2020). Determination of Secondary and Minor Plant Nutrients in Fertilizers by Atomic Absorption Spectrophotometry: Third Collaborative Study. Journal of Association of Official Analytical Chemists, 50(2), 401–407. https://doi.org/10.1093/jaoac/50.2.401.
Molinuevo-Salces, B., Ahring, B.K. &Uellendahl, H. (2015). Optimization of the co-digestion of catch crops with manure using a central composite design and reactor operation. Applied biochemistry and biotechnology, 175,1710-1723. 10.1007/s12010-014-1391-3.
Nkhata, S. G., Ayua, E., Kamau, E. H. & Shingiro, J. B. (2018). Fermentation and germination improve nutritional value of cereals and legumes through activation of endogenous enzymes. Food Science & Nutrition, 6(8), 2446–2458. https://doi.org/10.1002/fsn3.846.
Nielsen, P. M., Petersen, D. & Dambmann, C. (2001). Improved Method for Determining Food Protein Degree of Hydrolysis. Food chemistry and toxicology 66:5. https://doi.org/10.1111/j.1365-2621.2001.tb04614.x
Oreopoulou, V. & Russ, W. (2006). Utilization of Byproducts and Treatment of Waste in the Food Industry. Springer Science & Business Media.
Patsios, S. I., Dedousi, A., Sossidou, E. Ν. & Zdragas, A. (2020). Sustainable Animal Feed Protein through the Cultivation of YARROWIA Lipolytica on Agro-Industrial Wastes and byproducts. Sustainability: Science Practice and Policy, 12(4), 1398. https://doi.org/10.3390/su12041398.
Ravindran, B., Wong, J. W. C., Selvam, A., Thirunavukarasu, K. & Sekaran, G. (2016). Microbial biodegradation of proteinaceous tannery solid waste and production of a novel value-added product - Metalloprotease. Bioresource Technology, 217, 150–156. 10.1016/j.biortech.2016.03.033.
Samuel, R.A., Dash, S.S., Ali, L. Riyas. & Paari, K.A. (2021). Formulation and characterization of plant, animal, and probiotic based fish meals and evaluating their efficacy on growth and performance in zebrafish (danio rerio). Advances in Animal and Veterinary Sciences, 9(8)
Silva, J.F.X., Ribeiro, K., Silva, J.F., Cahú, T.B. & Bezerra, R.S. (2014). Utilization of tilapia processing waste for the production of fish protein hydrolysate. Animal feed science and technology, 196, 96-106. https://doi.org/10.1016/j.anifeedsci.2014.06.010
Simat, V. (2021). Valorization of seafood processing byproducts. In Valorization of agri-food wastes and byproducts. Agricultural and biological sciences, 515-536.
Shyam, S.S. & Akhila, K. (2022). Domestic fish consumption in India: Challenges and opportunities, Shrimp farming – made better for the Future ,10-25.
Solanki, P., Putatunda, C., Kumar, A., Bhatia, R. & Walia, A. (2021). Microbial proteases: ubiquitous enzymes with innumerable uses. 3 Biotech, 11(10), 428. https://doi.org/10.1007/s13205-021-02928-z.
Tropea, A., Potortì, A. G., Lo Turco, V., Russo, E., Vadalà, R., Rando, R. & Di Bella, G. (2021). Aquafeed Production from Fermented Fish Waste and Lemon Peel. Fermentation, 7(4), 272. https://doi.org/10.3390/fermentation7040272.
Tennalli, G.B., Garawadmath, S., Sequeira, L., Murudi, S., Patil, V., Divate, M.N.& Hungund, B.S. (2022). Media optimization for the production of alkaline protease by Bacillus cereus PW3A using response surface methodology. Journal of Applied Biology and Biotechnology, 1,10(4)-17-26.
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How to Cite
Bacillus cereus-mediated biofermentation of Sardine offal waste: A novel approach to enhance nutritional value by Response Surface Methodology optimization. (2024). Journal of Applied and Natural Science, 16(1), 158-171. https://doi.org/10.31018/jans.v16i1.5264
