Solid-State Fermentation of Distiller’s Dried Grains with Solubles Improves Digestibility for European Seabass (Dicentrarchus labrax) Juveniles
Abstract
:1. Introduction
2. Material and Methods
2.1. Solid-State Fermentation (SSF)
2.2. SSF Scale-Up
2.3. Experimental Diets
2.4. Digestibility Trial
2.5. Chemical Analyses
2.6. Enzymes Activity Analyses
2.6.1. Lignocellulolytic Enzymes
2.6.2. Digestive Enzymes Activity
2.7. Statistical Analyses
3. Results
3.1. Solid-State Fermentation
3.2. Diets and Ingredient Digestibility
4. Discussion
4.1. Solid-State Fermentation
4.2. Diets and Ingredient Digestibility
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- European Renewable Ethanol Renewable Ethanol Production by End-Use. Available online: https://epure.org/media/1929/renewable-ethanol-production-by-end-use-2018.jpg (accessed on 24 March 2020).
- Renewable Fuels Association. Ethanol & Co-Product Trade Exports and Imports. Available online: https://ethanolrfa.org/statistics/ethanol-co-product-trade/ (accessed on 24 March 2020).
- Renewable Fuels Association. Annual Ethanol Production U.S. and World Ethanol Production. Available online: https://ethanolrfa.org/markets-and-statistics/annual-ethanol-production (accessed on 24 March 2020).
- Rausch, K.D.; Belyea, R.L.; Ellersieck, M.R.; Singh, V.; Johnston, D.B.; Tumbleson, M.E. Particle Size Distributions of Ground Corn and DDGS from Dry Grind Processing. Trans. Am. Soc. Agric. Eng. 2005, 48, 273–277. [Google Scholar] [CrossRef]
- Bothast, R.J.; Schlicher, M.A. Biotechnological Processes for Conversion of Corn into Ethanol. Appl. Microbiol. Biotechnol. 2005, 67, 19–25. [Google Scholar] [CrossRef] [PubMed]
- Kwiatkowski, J.R.; McAloon, A.J.; Taylor, F.; Johnston, D.B. Modeling the Process and Costs of Fuel Ethanol Production by the Corn Dry-Grind Process. Ind. Crops Prod. 2006, 23, 288–296. [Google Scholar] [CrossRef]
- Ganesan, V.; Rosentrater, K.A.; Muthukumarappan, K. Methodology to Determine Soluble Content in Dry Grind Ethanol Coproduct Streams. Appl. Eng. Agric. 2006, 22, 899–903. [Google Scholar] [CrossRef]
- Renewable Fuels Association Feedstock Use and Co-Product Output. Available online: https://ethanolrfa.org/statistics/feedstock-use-co-product-output/ (accessed on 24 March 2020).
- Mohammadi Shad, Z.; Venkitasamy, C.; Wen, Z. Corn Distillers Dried Grains with Solubles: Production, Properties, and Potential Uses. Cereal Chem. 2021, 98, 999–1019. [Google Scholar] [CrossRef]
- FAO. The State of World Fisheries and Aquaculture 2022; FAO: Rome, Italy, 2022; ISBN 978-92-5-136364-5. [Google Scholar]
- Tacon, A.G.J.; Metian, M.; McNevin, A.A. Future Feeds: Suggested Guidelines for Sustainable Development. Rev. Fish. Sci. Aquac. 2022, 30, 135–142. [Google Scholar] [CrossRef]
- Belyea, R.L.; Rausch, K.D.; Tumbleson, M.E. Composition of Corn and Distillers Dried Grains with Solubles from Dry Grind Ethanol Processing. Bioresour. Technol. 2004, 94, 293–298. [Google Scholar] [CrossRef]
- Shurson, G.; Spiehs, M.; Whitney, M. The Use of Maize Distiller’s Dried Grains with Solubles in Pig Diets. Pig News Inf. 2004, 25, 75N–83N. [Google Scholar]
- Spiehs, M.J.; Whitney, M.H.; Shurson, G.C. Nutrient Database for Distiller’s Dried Grains with Solubles Produced from New Ethanol Plants in Minnesota and South Dakota. J. Anim. Sci. 2002, 80, 2639–2645. [Google Scholar] [CrossRef]
- Nuez Ortín, W.G.; Yu, P. Nutrient Variation and Availability of Wheat DDGS, Corn DDGS and Blend DDGS from Bioethanol Plants. J. Sci. Food Agric. 2009, 89, 1754–1761. [Google Scholar] [CrossRef]
- Lim, C.; Li, E.; Klesius, P.H. Distiller’s Dried Grains with Solubles as an Alternative Protein Source in Diets of Tilapia. Rev. Aquac. 2011, 3, 172–178. [Google Scholar] [CrossRef]
- Cozannet, P.; Primot, Y.; Gady, C.; Métayer, J.P.; Lessire, M.; Skiba, F.; Noblet, J. Energy Value of Wheat Distillers Grains with Solubles for Growing Pigs and Adult Sows. J. Anim. Sci. 2010, 88, 2382–2392. [Google Scholar] [CrossRef]
- Shelby, R.A.; Lim, C.; Yildrim-Aksoy, M.; Klesius, P.H. Effect of Distillers Dried Grains with Solubles-Incorporated Diets on Growth, Immune Function and Disease Resistance in Nile Tilapia (Oreochromis niloticus L.). Aquac. Res. 2008, 39, 1351–1353. [Google Scholar] [CrossRef]
- Shurson, J.; Noll, S.L. Feed and Alternative Uses for DDGs. In Proceedings of the Energy from Agriculture: New Technologies, Innovative Programs & Success Stories, St. Louis, MO, USA, 14–15 December 2005; pp. 1–11. [Google Scholar]
- Iram, A.; Cekmecelioglu, D.; Demirci, A. Distillers’ Dried Grains with Solubles (DDGS) and Its Potential as Fermentation Feedstock. Appl. Microbiol. Biotechnol. 2020, 104, 6115–6128. [Google Scholar] [CrossRef]
- Stein, H.H.; Shurson, G.C. Board-Invited Review: The Use and Application of Distillers Dried Grains with Solubles in Swine Diets. J. Anim. Sci. 2009, 87, 1292–1303. [Google Scholar] [CrossRef]
- Coyle, S.D.; Mengel, G.J.; Tidwell, J.H.; Webster, C.D. Evaluation of Growth, Feed Utilization, and Economics of Hybrid Tilapia, Oreochromis niloticus x Oreochromis aureus, Fed Diets Containing Different Protein Sources in Combination with Distillers Dried Grains with Solubles. Aquac. Res. 2004, 35, 365–370. [Google Scholar] [CrossRef]
- Schaeffer, T.W.; Brown, M.L.; Rosentrate, K.A. Performance Characteristics of Nile Tilapia (Oreochromis niloticus) Fed Diets Containing Graded Levels of Fuel-Based Distillers Dried Grains with Solubles. J. Aquac. Feed. Sci. Nutr. 2009, 1, 78–83. [Google Scholar] [CrossRef]
- Zhou, P.; Zhang, W.; Davis, D.A.; Lim, C. Growth Response and Feed Utilization of Juvenile Hybrid Catfish Fed Diets Containing Distiller’s Dried Grains with Solubles to Replace a Combination of Soybean Meal and Corn Meal. N. Am. J. Aquac. 2010, 72, 298–303. [Google Scholar] [CrossRef]
- Lim, C.; Yildirim-Aksoy, M.; Klesius, P.H. Growth Response and Resistance to Edwardsiella Ictaluri of Channel Catfish, Ictalurus Punctatus, Fed Diets Containing Distiller’s Dried Grains with Solubles. J. World Aquac. Soc. 2009, 40, 182–193. [Google Scholar] [CrossRef]
- Cheng, Z.J.; Hardy, R.W. Nutritional Value of Diets Containing Distiller’s Dried Grain with Solubles for Rainbow Trout, Oncorhynchus mykiss. J. Appl. Aquac. 2004, 15, 101–113. [Google Scholar] [CrossRef]
- Diógenes, A.F.; Basto, A.; Estevão-Rodrigues, T.T.; Moutinho, S.; Aires, T.; Oliva-Teles, A.; Peres, H. Soybean Meal Replacement by Corn Distillers Dried Grains with Solubles (DDGS) and Exogenous Non-Starch Polysaccharidases Supplementation in Diets for Gilthead Seabream (Sparus aurata) Juveniles. Aquaculture 2019, 500, 435–442. [Google Scholar] [CrossRef]
- Diógenes, A.F.; Castro, C.; Miranda, A.C.; Oliva-Teles, A.; Peres, H. Dietary Replacement of Fishmeal by Corn Distillers Dried Grains with Solubles (DDGS) in Diets for Turbot (Scophthalmus maximus, Linneaus, 1758) Juveniles. Aquaculture 2018, 492, 113–122. [Google Scholar] [CrossRef]
- Goda, A.M.A.S.; Ahmed, S.R.; Nazmi, H.M.; Aboseif, A.M.; Taha, M.K.S.; Fadda, S.H.; Baromh, M.Z.; El-Haroun, E.; Davies, S.J. Assessment of a High Protein Distillers Dried Grain (HP-DDG) Augmented with Phytase in Diets for European Sea Bass, Dicentrarchus Labrax Fingerlings on Growth Performance, Haematological Status, Immune Response and Related Gut and Liver Histology. Aquaculture 2020, 529, 735617. [Google Scholar] [CrossRef]
- Overland, M.; Krogdahl, Å.; Shurson, G.; Skrede, A.; Denstadli, V. Evaluation of Distiller’s Dried Grains with Solubles (DDGS) and High Protein Distiller’s Dried Grains (HPDDG) in Diets for Rainbow Trout (Oncorhynchus mykiss). Aquaculture 2013, 416–417, 201–208. [Google Scholar] [CrossRef]
- Diógenes, A.F.; Castro, C.; Carvalho, M.; Magalhães, R.; Estevão-Rodrigues, T.T.; Serra, C.R.; Oliva-Teles, A.; Peres, H. Exogenous Enzymes Supplementation Enhances Diet Digestibility and Digestive Function and Affects Intestinal Microbiota of Turbot (Scophthalmus maximus) Juveniles Fed Distillers’ Dried Grains with Solubles (DDGS) Based Diets. Aquaculture 2018, 486, 42–50. [Google Scholar] [CrossRef]
- Parmar, A.; Patel, V.; Usadadia, S.; Rathwa, S.; Prajapati, D. A Solid State Fermentation, Its Role in Animal Nutrition: A Review. Int. J. Chem. Stud. 2019, 7, 4626–4633. [Google Scholar]
- Graminha, E.B.N.; Gonçalves, A.Z.L.; Pirota, R.D.P.B.; Balsalobre, M.A.A.; da Silva, R.; Gomes, E. Enzyme Production by Solid-State Fermentation: Application to Animal Nutrition. Anim. Feed Sci. Technol. 2008, 144, 1–22. [Google Scholar] [CrossRef]
- Yang, S.; Lio, J.Y.; Wang, T. Evaluation of Enzyme Activity and Fiber Content of Soybean Cotyledon Fiber and Distiller’s Dried Grains with Solubles by Solid State Fermentation. Appl. Biochem. Biotechnol. 2012, 167, 109–121. [Google Scholar] [CrossRef]
- Fleuri, L.F.; Kawaguti, H.Y.; Pedrosa, V.A.; Vianello, F.; Lima, G.P.P.; Novelli, P.K.; Okino-Delgado, C.H. Exploration of Microorganisms Producing Bioactive Molecules of Industrial Interest by Solid State Fermentation. In Food Quality, Safety and Technology; Springer: Vienna, Austria, 2013; pp. 147–161. [Google Scholar]
- Sharma, R.K.; Arora, D.S. Fungal Degradation of Lignocellulosic Residues: An Aspect of Improved Nutritive Quality. Crit. Rev. Microbiol. 2015, 41, 52–60. [Google Scholar] [CrossRef]
- Fernandes, H.; Moyano, F.; Castro, C.; Salgado, J.; Martínez, F.; Aznar, M.; Fernandes, N.; Ferreira, P.; Gonçalves, M.; Belo, I.; et al. Solid-State Fermented Brewer’s Spent Grain Enzymatic Extract Increases in Vitro and in Vivo Feed Digestibility in European Seabass. Sci. Rep. 2021, 11, 22946. [Google Scholar] [CrossRef]
- Wang, C.; Su, W.; Zhang, Y.; Hao, L.; Wang, F.; Lu, Z.; Zhao, J.; Liu, X.; Wang, Y. Solid-State Fermentation of Distilled Dried Grain with Solubles with Probiotics for Degrading Lignocellulose and Upgrading Nutrient Utilization. AMB Express 2018, 8, 1–13. [Google Scholar] [CrossRef]
- Naylor, R.L.; Hardy, R.W.; Bureau, D.P.; Chiu, A.; Elliott, M.; Farrell, A.P.; Forster, I.; Gatlin, D.M.; Goldburg, R.J.; Hua, K.; et al. Feeding Aquaculture in an Era of Finite Resources. Proc. Natl. Acad. Sci. USA 2009, 106, 15103–15110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schuster, E.; Dunn-Coleman, N.; Frisvad, J.; van Dijck, P. On the Safety of Aspergillus Niger—A Review. Appl. Microbiol. Biotechnol. 2002, 59, 426–435. [Google Scholar]
- Serra, R.; Cabañes, F.J.; Perrone, G.; Castellá, G.; Venâncio, A.; Mulè, G.; Kozakiewicz, Z. Aspergillus Ibericus: A New Species of Section Nigri Isolated from Grapes. Mycologia 2006, 98, 295–306. [Google Scholar] [CrossRef]
- Cho, C.Y.; Slinger, S.J.; Bayley, H.S. Bioenergetics of Salmonid Fishes: Energy Intake, Expenditure and Productivity. Comp. Biochem. Physiol. Part B Comp. Biochem. 1982, 73, 25–41. [Google Scholar] [CrossRef]
- Association of Official Analytical Chemists; Horwitz, W.; Association of Official Agricultural Chemists (U.S.). Official Methods of Analysis of the Association of Official Analytical Chemists; The Association: New York, NY, USA, 1980; ISBN 0935584145. [Google Scholar]
- Fiske, C.; Chem, Y.S. The Colorimetric Determination of Phosphorus. J. Biol. Chem. 1925, 66, 375–400. [Google Scholar] [CrossRef]
- Beutler, H. Methods of Enzymatic Analysis. In Methods of Enzymatic Analysis; Elsevier: Amsterdam, The Netherlands, 1984; pp. 2–10. [Google Scholar]
- Furukawa, A.; Tsukahara, H. On the Acid Digestion Method for the Determination of Chromic Oxide as an Index Substance in the Study of Digestibility of Fish Feed. Bull. Jpn. Soc. Sci. Fish. 1966, 32, 502–508. [Google Scholar] [CrossRef]
- Leite, P.; Salgado, J.M.; Venâncio, A.; Domínguez, J.M.; Belo, I. Ultrasounds Pretreatment of Olive Pomace to Improve Xylanase and Cellulase Production by Solid-State Fermentation. Bioresour. Technol. 2016, 214, 737–746. [Google Scholar] [CrossRef]
- Miller, G.L. Modified DNS Method for Reducing Sugars. Anal. Chem. 1959, 31, 426–428. [Google Scholar] [CrossRef]
- Bradford, M. A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef]
- Moutinho, S.; Peres, H.; Serra, C.; Martínez-Llorens, S.; Tomás-Vidal, A.; Jover-Cerdá, M.; Oliva-Teles, A. Meat and Bone Meal as Partial Replacement of Fishmeal in Diets for Gilthead Sea Bream (Sparus aurata) Juveniles: Diets Digestibility, Digestive Function, and Microbiota Modulation. Aquaculture 2017, 479, 721–731. [Google Scholar] [CrossRef]
- El-Bakry, M.; Abraham, J.; Cerda, A.; Barrena, R.; Ponsá, S.; Gea, T.; Sánchez, A. From Wastes to High Value Added Products: Novel Aspects of SSF in the Production of Enzymes. Crit. Rev. Environ. Sci. Technol. 2015, 45, 1999–2042. [Google Scholar] [CrossRef]
- Leite, P.; Sousa, D.; Fernandes, H.; Ferreira, M.; Costa, A.R.; Filipe, D.; Gonçalves, M.; Peres, H.; Belo, I.; Salgado, J.M. Recent Advances in Production of Lignocellulolytic Enzymes by Solid-State Fermentation of Agro-Industrial Wastes. Curr. Opin. Green Sustain. Chem. 2021, 27, 100407. [Google Scholar] [CrossRef]
- Mansour, A.A.; Arnaud, T.; Lu-Chau, T.A.; Fdz-Polanco, M.; Moreira, M.T.; Rivero, J.A.C. Review of Solid State Fermentation for Lignocellulolytic Enzyme Production: Challenges for Environmental Applications. Rev. Environ. Sci. Biotechnol. 2016, 15, 31–46. [Google Scholar] [CrossRef]
- Salgado, J.M.; Abrunhosa, L.; Venâncio, A.; Domínguez, J.M.; Belo, I. Screening of Winery and Olive Mill Wastes for Lignocellulolytic Enzyme Production from Aspergillus Species by Solid-State Fermentation. Biomass Convers. Biorefin. 2014, 4, 201–209. [Google Scholar] [CrossRef]
- Fernandes, H.; Salgado, J.M.; Ferreira, M.; Vršanská, M.; Fernandes, N.; Castro, C.; Oliva-Teles, A.; Peres, H.; Belo, I. Valorization of Brewer’s Spent Grain Using Biological Treatments and Its Application in Feeds for European Seabass (Dicentrarchus labrax). Front. Bioeng. Biotechnol. 2022, 10, 732948. [Google Scholar] [CrossRef]
- Filipe, D.; Fernandes, H.; Castro, C.; Peres, H.; Oliva-Teles, A.; Belo, I.; Salgado, J.M. Improved Lignocellulolytic Enzyme Production and Antioxidant Extraction Using Solid-State Fermentation of Olive Pomace Mixed with Winery Waste. Biofuels Bioprod. Biorefining 2020, 14, 78–91. [Google Scholar] [CrossRef]
- Dashtban, M.; Schraft, H.; Qin, W. Fungal Bioconversion of Lignocellulosic Residues; Opportunities & Perspectives. Int. J. Biol. Sci. 2009, 5, 578. [Google Scholar]
- Iram, A.; Cekmecelioglu, D.; Demirci, A. Screening of Bacterial and Fungal Strains for Cellulase and Xylanase Production Using Distillers’ Dried Grains with Solubles (DDGS) as the Main Feedstock. Biomass Convers. Biorefin. 2020, 11, 1955–1964. [Google Scholar] [CrossRef]
- Jönsson, L.J.; Martín, C. Pretreatment of Lignocellulose: Formation of Inhibitory by-Products and Strategies for Minimizing Their Effects. Bioresour. Technol. 2016, 199, 103–112. [Google Scholar] [CrossRef]
- Fernandes, H.; Salgado, J.M.; Martins, N.; Peres, H.; Oliva-Teles, A.; Belo, I. Sequential Bioprocessing of Ulva Rigida to Produce Lignocellulolytic Enzymes and to Improve Its Nutritional Value as Aquaculture Feed. Bioresour. Technol. 2019, 281, 277–285. [Google Scholar] [CrossRef]
- Li, W.; Zhao, L.; He, X. Degradation Potential of Different Lignocellulosic Residues by Trichoderma longibrachiatum and Trichoderma afroharzianum under Solid State Fermentation. Process Biochem. 2022, 112, 6–17. [Google Scholar] [CrossRef]
- Terefe, Z.K.; Omwamba, M.N.; Nduko, J.M. Effect of Solid State Fermentation on Proximate Composition, Antinutritional Factors and in Vitro Protein Digestibility of Maize Flour. Food Sci. Nutr. 2021, 9, 6343–6352. [Google Scholar] [CrossRef] [PubMed]
- Adebo, O.A.; Medina-Meza, I.G. Impact of Fermentation on the Phenolic Compounds and Antioxidant Activity of Whole Cereal Grains: A Mini Review. Molecules 2020, 25, 927. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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. 2012, 5, 2697–2707. [Google Scholar] [CrossRef]
- Sánchez, C. Lignocellulosic Residues: Biodegradation and Bioconversion by Fungi. Biotechnol. Adv. 2009, 27, 185–194. [Google Scholar] [CrossRef]
- Fan, W.; Huang, X.; Liu, K.; Xu, Y.; Hu, B.; Chi, Z. Nutrition Component Adjustment of Distilled Dried Grain with Solubles via Aspergillus Niger and Its Change about Dynamic Physiological Metabolism. Fermentation 2022, 8, 264. [Google Scholar] [CrossRef]
- Omarini, A.B.; Labuckas, D.; Zunino, M.P.; Pizzolitto, R.; Fernández-Lahore, M.; Barrionuevo, D.; Zygadlo, J.A. Upgrading the Nutritional Value of Rice Bran by Solid-State Fermentation with Pleurotus sapidus. Fermentation 2019, 5, 44. [Google Scholar] [CrossRef]
- 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. 2011, 29, 365–373. [Google Scholar] [CrossRef]
- Chen, G.; Chen, B.; Song, D. Co-Microbiological Regulation of Phenolic Release through Solid-State Fermentation of Corn Kernels (Zea Mays L.) to Improve Their Antioxidant Activity. LWT 2021, 142, 111003. [Google Scholar] [CrossRef]
- Fernandes, H.; Martins, N.; Vieira, L.; Salgado, J.M.; Castro, C.; Oliva-Teles, A.; Belo, I.; Peres, H. Pre-Treatment of Ulva Rigida Improves Its Nutritional Value for European Seabass (Dicentrarchus labrax) Juveniles. Algal Res. 2022, 66, 102803. [Google Scholar] [CrossRef]
- Buenavista, R.M.E.; Siliveru, K.; Zheng, Y. Utilization of Distiller’s Dried Grains with Solubles: A Review. J. Agric. Food Res. 2021, 5, 100195. [Google Scholar] [CrossRef]
- Enes, P.; Panserat, S.; Kaushik, S.; Oliva-Teles, A. Dietary Carbohydrate Utilization by European Sea Bass (Dicentrarchus labrax L.) and Gilthead Sea Bream (Sparus aurata L.) Juveniles. Rev. Fish. Sci. 2011, 19, 201–215. [Google Scholar] [CrossRef]
- Sinha, A.K.; Kumar, V.; Makkar, H.P.S.; de Boeck, G.; Becker, K. Non-Starch Polysaccharides and Their Role in Fish Nutrition—A Review. Food Chem. 2011, 127, 1409–1426. [Google Scholar] [CrossRef]
- Castro, C.; Peréz-Jiménez, A.; Coutinho, F.; Díaz-Rosales, P.; Alexandra, C.; Serra, R.; Panserat, S.; Corraze, G.; Peres, H.; Oliva-Teles, A. Dietary Carbohydrate and Lipid Sources Affect Differently the Oxidative Status of European Sea Bass (Dicentrarchus labrax) Juveniles. Br. J. Nutr. 2015, 114, 1584–1593. [Google Scholar] [CrossRef]
- Castillo, S.; Gatlin, D.M. Dietary Supplementation of Exogenous Carbohydrase Enzymes in Fish Nutrition: A Review. Aquaculture 2015, 435, 286–292. [Google Scholar] [CrossRef]
- Magalhães, R.; Coutinho, F.; Pousão-Ferreira, P.; Aires, T.; Oliva-Teles, A.; Peres, H. Corn Distiller’s Dried Grains with Solubles: Apparent Digestibility and Digestive Enzymes Activities in European Seabass (Dicentrarchus labrax) and Meagre (Argyrosomus regius). Aquaculture 2015, 443, 90–97. [Google Scholar] [CrossRef]
- Azm, F.R.A.; Kong, F.; Tan, Q.; Zhu, Y.; Yu, H.; Yao, J.; Luo, Z. Effects of Replacement of Dietary Rapeseed Meal by Distiller’s Dried Grains with Solubles (DDGS) on Growth Performance, Muscle Texture, Health and Expression of Muscle-Related Genes in Grass Carp (Ctenopharyngodon idellus). Aquaculture 2021, 533, 736169. [Google Scholar]
- Bedford, M.R.; Cowieson, A.J. Exogenous Enzymes and Their Effects on Intestinal Microbiology. Anim. Feed Sci. Technol. 2012, 173, 76–85. [Google Scholar] [CrossRef]
- Zheng, C.C.; Wu, J.W.; Jin, Z.H.; Ye, Z.F.; Yang, S.; Sun, Y.Q.; Fei, H. Exogenous Enzymes as Functional Additives in Finfish Aquaculture. Aquac. Nutr. 2020, 26, 213–224. [Google Scholar] [CrossRef]
- Davies, S.J.; El-Haroun, E.R.; Hassaan, M.S.; Bowyer, P.H. A Solid-State Fermentation (SSF) Supplement Improved Performance, Digestive Function and Gut Ultrastructure of Rainbow Trout (Oncorhynchus mykiss) Fed Plant Protein Diets Containing Yellow Lupin Meal. Aquaculture 2021, 545, 737177. [Google Scholar] [CrossRef]
- Deng, J.; Zhang, X.; Sun, Y.; Mi, H.; Zhang, L. Effects of Different Types of Non-Starch Polysaccharides on Growth, Digestive Enzyme Activity, Intestinal Barrier Function and Antioxidant Activity of Rainbow Trout (Oncorhynchus mykiss). Aquac. Rep. 2021, 21, 100864. [Google Scholar] [CrossRef]
- Glencross, B.; Rutherford, N.; Bourne, N. The Influence of Various Starch and Non-Starch Polysaccharides on the Digestibility of Diets Fed to Rainbow Trout (Oncorhynchus mykiss). Aquaculture 2012, 356, 141–146. [Google Scholar] [CrossRef]
- Magalhães, R.; Díaz-Rosales, P.; Diógenes, A.F.; Enes, P.; Oliva-Teles, A.; Peres, H. Improved Digestibility of Plant Ingredient-Based Diets for European Seabass (Dicentrarchus Labrax) with Exogenous Enzyme Supplementation. Aquac. Nutr. 2018, 24, 1287–1295. [Google Scholar] [CrossRef]
- Magalhães, R.; Lopes, T.; Martins, N.; Díaz-Rosales, P.; Couto, A.; Pousão-Ferreira, P.; Oliva-Teles, A.; Peres, H. Carbohydrases Supplementation Increased Nutrient Utilization in White Seabream (Diplodus sargus) Juveniles Fed High Soybean Meal Diets. Aquaculture 2016, 463, 43–50. [Google Scholar] [CrossRef]
- Lin, S.; Mai, K.; Tan, B. Effects of Exogenous Enzyme Supplementation in Diets on Growth and Feed Utilization in Tilapia, Oreochromis niloticus x O. Aureus. Aquac Res 2007, 38, 1645–1653. [Google Scholar] [CrossRef]
- Liang, C.H.; Syu, J.L.; Mau, J.L. Antioxidant Properties of Solid-State Fermented Adlay and Rice by Phellinus linteus. Food Chem. 2009, 116, 841–845. [Google Scholar] [CrossRef]
- Jiang, T.; Feng, L.; Liu, Y.; Jiang, W.; Jiang, J.; Li, S.; Tang, L.; Kuang, S.; Zhou, X. Effects of Exogenous Xylanase Supplementation in Plant Protein-enriched Diets on Growth Performance, Intestinal Enzyme Activities and Microflora of Juvenile J Ian Carp (Cyprinus carpio Var. J Ian). Aquac. Nutr. 2014, 20, 632–645. [Google Scholar] [CrossRef]
- Xavier, B.; Sahu, N.P.; Pal, A.K.; Jain, K.K.; Misra, S.; Dalvi, R.S.; Baruah, K. Water Soaking and Exogenous Enzyme Treatment of Plant-Based Diets: Effect on Growth Performance, Whole-Body Composition, and Digestive Enzyme Activities of Rohu, Labeo rohita (Hamilton), Fingerlings. Fish. Physiol. Biochem. 2012, 38, 341–353. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Y.; Yuan, X.; Liang, X.-F.; Fang, L.; Li, J.; Guo, X.; Bai, X.; He, S. Enhancement of Growth and Intestinal Flora in Grass Carp: The Effect of Exogenous Cellulase. Aquaculture 2013, 416, 1–7. [Google Scholar] [CrossRef]
- Shi, X.; Luo, Z.; Chen, F.; Wei, C.; Wu, K.; Zhu, X.; Liu, X. Effect of Fish Meal Replacement by Chlorella Meal with Dietary Cellulase Addition on Growth Performance, Digestive Enzymatic Activities, Histology and Myogenic Genes’ Expression for Crucian Carp Carassius auratus. Aquac. Res. 2017, 48, 3244–3256. [Google Scholar] [CrossRef]
Fishmeal 1 | DDGS 2 | SSF-DDGS 3 | |
---|---|---|---|
Dry matter (%; DM) | 85.8 | 85.3 | 95.5 |
Ash | 10.6 | 3.8 | 5.1 |
Crude Protein | 77.5 | 26.7 | 30.1 |
Crude Lipids | 7.6 | 3.4 | 4.3 |
Cellulose | — | 40.5 | 17.6 |
Hemicellulose | — | 22.9 | 22.4 |
Lignin | — | 17.6 | 17.6 |
Acid Detergent Fiber | — | 28.2 | 35.3 |
Neutral Detergent Fiber | — | 63.1 | 57.6 |
Starch | — | 0.8 | 0.7 |
Phosphorus | 2.4 | 0.6 | 0.6 |
Gross energy (kJ/g DM) | 18.2 | 19.8 | 20.1 |
Cellulase | — | — | 43.4 |
Xylanase | — | — | 68 |
Diets | Reference | DDGS | SSF-DDGS |
---|---|---|---|
Ingredients | |||
Fishmeal 1 | 63.2 | 44.2 | 44.2 |
DDGS 2 | ― | 30 | ― |
SSF-DDGS 3 | ― | ― | 30 |
Pre-gelatinized corn starch 4 | 22.1 | 15.4 | 15.4 |
Fish oil | 10.2 | 7.2 | 7.2 |
Vitamins premix 5 | 1 | 0.7 | 0.7 |
Choline chloride (50%) | 0.5 | 0.4 | 0.4 |
Mineral premix 6 | 1 | 0.7 | 0.7 |
Chromium oxide | 1 | 0.7 | 0.7 |
Binder 7 | 1 | 0.7 | 0.7 |
Proximate analysis | |||
Dry matter (%) | 94.3 | 93.3 | 93.5 |
Crude protein | 47.9 | 40.6 | 42.6 |
Crude lipids | 14.6 | 12.6 | 12 |
Ash | 14.6 | 13.3 | 14.2 |
Phosphorus | 0.8 | 0.7 | 0.7 |
Cellulose | ― | 12.2 | 8.5 |
Starch | 20.4 | 19.2 | 19.9 |
Gross energy (kJ/g) | 20.2 | 20.6 | 20.8 |
Chromium oxide | 0.76 | 0.56 | 0.55 |
After SSF | ||||
---|---|---|---|---|
Unfermented | A. ibericus | A. uvarum | A. carbonarius | |
Total nitrogen | 42.7 ± 1.1 | 49.7 ± 0.7 | 34.0 ± 2.2 | 44.9 ± 0.5 |
Soluble Protein | 0.28 a ± 0.00 | 5.27 b ± 0.24 | 5.31 b ± 0.69 | 4.71 b ± 0.15 |
Total phenols (mg caffeic acid/kg DM) | 1.49 a ± 0.03 | 4.86 b ± 0.03 | 5.06 b ± 0.49 | 9.57 c ± 0.02 |
Reducing sugars (mg/kg DM) | 9.47 a ± 0.45 | 31.9 b ± 0.74 | 28.4 b ± 1.8 | 38.1 c ± 0.60 |
Hemicellulose | 229.3 a ± 2.1 | 242.9 a ± 15.1 | 149.0 b ± 17.1 | 209.1 ab ± 20.9 |
Cellulose | 405.2 a ± 19.6 | 204.4 b ± 6.4 | 165.4 b ± 11.0 | 212 b ± 20.2 |
Lignin | 176.4 a ± 11.0 | 129.0 b ± 0.0 | 240.7 c ± 5.9 | 171.4 a ± 10.2 |
NDF | 810.9 a ± 16.8 | 576.3 ab ± 15.2 | 592.5 ab ± 25.2 | 555.1 b ± 26.1 |
ADF | 581.6 a ± 0.2 | 333.4 b ± 4.6 | 383.4 ab ± 7.1 | 406.1 ab ± 14.0 |
Ash | 38.1 ± 2.5 | 54.3 ± 3.1 | 43.5 ± 8.3 | 54.9 ± 1.1 |
Enzymatic activity | ||||
Xylanase | ― | 68.0 ab ± 2.05 | 152.1 b ± 42.31 | 31.2 a ± 1.0 |
Cellulase | ― | 44.6 a ± 1.58 | 27.4 b ± 7.17 | 3.75 c ± 1.46 |
Diets | Reference | DDGS | SSF-DDGS | SEM |
---|---|---|---|---|
Dry matter | 83.7 b | 74.9 a | 75.1 a | 0.6 |
Organic matter | 85.1 b | 75.2 a | 75.1 a | 0.7 |
Protein | 91.9 | 91.9 | 93.6 | 0.4 |
Lipids | 98.9 c | 93.4 a | 96.0 b | 0.7 |
Starch | 88.1 b | 79.3 a | 81.8 a | 0.5 |
Energy | 93.9 b | 86.8 a | 92.7 b | 1.2 |
Phosphorus | 92 | 87.2 | 88.4 | 1.1 |
Ingredients | DDGS | SSF-DDGS | SEM |
---|---|---|---|
Dry matter | 54.6 | 54 | 2.1 |
Organic matter | 54.3 | 55.2 | 2.1 |
Protein | 88.5 | 96.6 * | 2 |
Lipids | 87.9 | 98.6 * | 2.4 |
Starch | 58.8 | 65.3 * | 2.7 |
Energy | 70 | 89.9 * | 1.3 |
Phosphorus | 73.4 | 77.5 | 1.7 |
Diets | Reference | DDGS | SSF-DDGS | SEM | ||
---|---|---|---|---|---|---|
Total proteases | ||||||
Anterior intestine | 467.4 | 487.4 | 422.2 | 13.7 | ||
Distal intestine | 342.6 | 302.9 | 403.9 | 21.1 | ||
Trypsin | ||||||
Anterior intestine | 5.4 | 10.5 | 12.8 | 0.9 | ||
Distal intestine | 10.9 | 17 | 16.4 | 1.2 | ||
Chymotrypsin | ||||||
Anterior intestine | 694.3 | 1192.8 | 1283.4 | 70.7 | ||
Distal intestine | 976.2 | 1469.8 | 1336.3 | 71.2 | ||
Lipase | ||||||
Anterior intestine | 365.9 a | 497.0 ab | 541.2 b | 0.5 | ||
Distal intestine | 478.4 a | 864.6 b | 694.6 b | 0.5 | ||
Amylase | ||||||
Anterior intestine | 6.2 | 7.1 | 6.5 | 30.3 | ||
Distal intestine | 6.7 | 9.8 | 6.5 | 44.3 | ||
Two-Way ANOVA 1 | ||||||
Diet | Intestine section | Interaction | Diets | |||
Reference | DDGS | SSF-DDGS | ||||
Proteases | ns | *** | * | ― | ― | ― |
Trypsin | *** | ** | ns | a | b | b |
Chymotrypsin | *** | ns | ns | a | b | b |
Lipases | *** | *** | * | ― | ― | ― |
Amylase | * | ns | ns | ab | c | b |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Filipe, D.; Dias, M.; Magalhães, R.; Fernandes, H.; Salgado, J.; Belo, I.; Oliva-Teles, A.; Peres, H. Solid-State Fermentation of Distiller’s Dried Grains with Solubles Improves Digestibility for European Seabass (Dicentrarchus labrax) Juveniles. Fishes 2023, 8, 90. https://doi.org/10.3390/fishes8020090
Filipe D, Dias M, Magalhães R, Fernandes H, Salgado J, Belo I, Oliva-Teles A, Peres H. Solid-State Fermentation of Distiller’s Dried Grains with Solubles Improves Digestibility for European Seabass (Dicentrarchus labrax) Juveniles. Fishes. 2023; 8(2):90. https://doi.org/10.3390/fishes8020090
Chicago/Turabian StyleFilipe, Diogo, Mário Dias, Rui Magalhães, Helena Fernandes, José Salgado, Isabel Belo, Aires Oliva-Teles, and Helena Peres. 2023. "Solid-State Fermentation of Distiller’s Dried Grains with Solubles Improves Digestibility for European Seabass (Dicentrarchus labrax) Juveniles" Fishes 8, no. 2: 90. https://doi.org/10.3390/fishes8020090
APA StyleFilipe, D., Dias, M., Magalhães, R., Fernandes, H., Salgado, J., Belo, I., Oliva-Teles, A., & Peres, H. (2023). Solid-State Fermentation of Distiller’s Dried Grains with Solubles Improves Digestibility for European Seabass (Dicentrarchus labrax) Juveniles. Fishes, 8(2), 90. https://doi.org/10.3390/fishes8020090