TLR2/TLR5 Signaling and Gut Microbiota Mediate Soybean-Meal-Induced Enteritis and Declined Growth and Antioxidant Capabilities in Large Yellow Croaker (<i>Larimichthys crocea</i>)
Soybean meal, renowned for its high yield, cost efficiency, and protein richness, serves as a pivotal plant-based alternative to fish meal. However, high soybean meal inclusion in <i>Larimichthys crocea</i> diets is linked to enteritis and oxidative damage, with unknown mechanisms. Our s...
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2024-11-01
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| author | Lei Zheng Chao Zeng Wanqin Zhu Jiaonan Zhang Lei Wang Jianchun Shao Wei Zhao |
| author_facet | Lei Zheng Chao Zeng Wanqin Zhu Jiaonan Zhang Lei Wang Jianchun Shao Wei Zhao |
| author_sort | Lei Zheng |
| collection | DOAJ |
| description | Soybean meal, renowned for its high yield, cost efficiency, and protein richness, serves as a pivotal plant-based alternative to fish meal. However, high soybean meal inclusion in <i>Larimichthys crocea</i> diets is linked to enteritis and oxidative damage, with unknown mechanisms. Our study aims to elucidate the molecular basis of soybean-meal-induced enteritis and its impact on intestinal microbiota in <i>L. crocea</i>. To this end, four isonitrogenous and isolipidic diets with varying soybean meal levels (0% FM, 15% SBM15, 30% SBM30, and 45% SBM45) were administered to <i>L. crocea</i> for 8 weeks. The results indicated that the SBM30 and SBM45 treatments significantly hindered fish growth, digestive efficiency, and protein utilization. Furthermore, high soybean meal levels (SBM30 and SBM45) activated intestinal Toll-like receptors (<i>TLR2A</i>, <i>TLR2B</i>, <i>TLR5</i>, and <i>TLR22</i>), stimulating C-Rel and mTOR protein expression and elevating ERK phosphorylation. This led to increased pro-inflammatory cytokine production (<i>IL-1β</i>, <i>IL-6</i>, and <i>TNF-α</i>) and decreased anti-inflammatory cytokine expression (<i>IL-4/13A</i>, <i>IL-4/13B</i>, and <i>TGF-β</i>), suggesting a potential signaling pathway for soybean-meal-induced enteritis. Furthermore, enteritis induced by high soybean meal levels led to oxidative damage, evident from increased MDA levels and decreased antioxidant enzyme activities (SOD and CAT). The SBM30 and SBM45 treatments increased Firmicutes and Bacteroidetes abundance in fish gut microbiota, while Proteobacteria abundance decreased. This microbiota shift may enhance soybean meal nutrient utilization, yet high soybean meal concentrations still impair growth. A soybean-meal-rich diet promotes harmful bacteria like <i>Rhodococcus</i> and depletes probiotics like <i>Ralstonia</i>, increasing disease risks. <i>L. crocea</i> has limited tolerance for soybean meal, necessitating advanced processing to mitigate anti-nutritional factors. Ultimately, exploring alternative protein sources beyond soybean meal for fish meal replacement is optimal for <i>L. crocea</i>. |
| format | Article |
| id | doaj-art-a004de2f951f4b4eae65b0778341fa92 |
| institution | Kabale University |
| issn | 2077-1312 |
| language | English |
| publishDate | 2024-11-01 |
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| series | Journal of Marine Science and Engineering |
| spelling | doaj-art-a004de2f951f4b4eae65b0778341fa922024-11-26T18:08:16ZengMDPI AGJournal of Marine Science and Engineering2077-13122024-11-011211201610.3390/jmse12112016TLR2/TLR5 Signaling and Gut Microbiota Mediate Soybean-Meal-Induced Enteritis and Declined Growth and Antioxidant Capabilities in Large Yellow Croaker (<i>Larimichthys crocea</i>)Lei Zheng0Chao Zeng1Wanqin Zhu2Jiaonan Zhang3Lei Wang4Jianchun Shao5Wei Zhao6Applied Technology Engineering Center of Fujian Provincial Higher Education for Marine Resource Protection and Ecological Governance, Xiamen Ocean Vocational College, Xiamen 361012, ChinaState Key Laboratory of Mariculture Breeding, Key Laboratory of Marine Biotechnology of Fujian Province, College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaState Key Laboratory of Mariculture Breeding, Key Laboratory of Marine Biotechnology of Fujian Province, College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaFujian Province Key Laboratory of Special Aquatic Formula Feed, Fujian Tianma Science and Technology Group Co., Ltd., Fuzhou 350300, ChinaInstitute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, ChinaState Key Laboratory of Mariculture Breeding, Key Laboratory of Marine Biotechnology of Fujian Province, College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaState Key Laboratory of Mariculture Breeding, Key Laboratory of Marine Biotechnology of Fujian Province, College of Marine Sciences, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaSoybean meal, renowned for its high yield, cost efficiency, and protein richness, serves as a pivotal plant-based alternative to fish meal. However, high soybean meal inclusion in <i>Larimichthys crocea</i> diets is linked to enteritis and oxidative damage, with unknown mechanisms. Our study aims to elucidate the molecular basis of soybean-meal-induced enteritis and its impact on intestinal microbiota in <i>L. crocea</i>. To this end, four isonitrogenous and isolipidic diets with varying soybean meal levels (0% FM, 15% SBM15, 30% SBM30, and 45% SBM45) were administered to <i>L. crocea</i> for 8 weeks. The results indicated that the SBM30 and SBM45 treatments significantly hindered fish growth, digestive efficiency, and protein utilization. Furthermore, high soybean meal levels (SBM30 and SBM45) activated intestinal Toll-like receptors (<i>TLR2A</i>, <i>TLR2B</i>, <i>TLR5</i>, and <i>TLR22</i>), stimulating C-Rel and mTOR protein expression and elevating ERK phosphorylation. This led to increased pro-inflammatory cytokine production (<i>IL-1β</i>, <i>IL-6</i>, and <i>TNF-α</i>) and decreased anti-inflammatory cytokine expression (<i>IL-4/13A</i>, <i>IL-4/13B</i>, and <i>TGF-β</i>), suggesting a potential signaling pathway for soybean-meal-induced enteritis. Furthermore, enteritis induced by high soybean meal levels led to oxidative damage, evident from increased MDA levels and decreased antioxidant enzyme activities (SOD and CAT). The SBM30 and SBM45 treatments increased Firmicutes and Bacteroidetes abundance in fish gut microbiota, while Proteobacteria abundance decreased. This microbiota shift may enhance soybean meal nutrient utilization, yet high soybean meal concentrations still impair growth. A soybean-meal-rich diet promotes harmful bacteria like <i>Rhodococcus</i> and depletes probiotics like <i>Ralstonia</i>, increasing disease risks. <i>L. crocea</i> has limited tolerance for soybean meal, necessitating advanced processing to mitigate anti-nutritional factors. Ultimately, exploring alternative protein sources beyond soybean meal for fish meal replacement is optimal for <i>L. crocea</i>.https://www.mdpi.com/2077-1312/12/11/2016<i>Larimichthys crocea</i>vegetable proteinenteritisoxidative damagegut microbiota |
| spellingShingle | Lei Zheng Chao Zeng Wanqin Zhu Jiaonan Zhang Lei Wang Jianchun Shao Wei Zhao TLR2/TLR5 Signaling and Gut Microbiota Mediate Soybean-Meal-Induced Enteritis and Declined Growth and Antioxidant Capabilities in Large Yellow Croaker (<i>Larimichthys crocea</i>) Journal of Marine Science and Engineering <i>Larimichthys crocea</i> vegetable protein enteritis oxidative damage gut microbiota |
| title | TLR2/TLR5 Signaling and Gut Microbiota Mediate Soybean-Meal-Induced Enteritis and Declined Growth and Antioxidant Capabilities in Large Yellow Croaker (<i>Larimichthys crocea</i>) |
| title_full | TLR2/TLR5 Signaling and Gut Microbiota Mediate Soybean-Meal-Induced Enteritis and Declined Growth and Antioxidant Capabilities in Large Yellow Croaker (<i>Larimichthys crocea</i>) |
| title_fullStr | TLR2/TLR5 Signaling and Gut Microbiota Mediate Soybean-Meal-Induced Enteritis and Declined Growth and Antioxidant Capabilities in Large Yellow Croaker (<i>Larimichthys crocea</i>) |
| title_full_unstemmed | TLR2/TLR5 Signaling and Gut Microbiota Mediate Soybean-Meal-Induced Enteritis and Declined Growth and Antioxidant Capabilities in Large Yellow Croaker (<i>Larimichthys crocea</i>) |
| title_short | TLR2/TLR5 Signaling and Gut Microbiota Mediate Soybean-Meal-Induced Enteritis and Declined Growth and Antioxidant Capabilities in Large Yellow Croaker (<i>Larimichthys crocea</i>) |
| title_sort | tlr2 tlr5 signaling and gut microbiota mediate soybean meal induced enteritis and declined growth and antioxidant capabilities in large yellow croaker i larimichthys crocea i |
| topic | <i>Larimichthys crocea</i> vegetable protein enteritis oxidative damage gut microbiota |
| url | https://www.mdpi.com/2077-1312/12/11/2016 |
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