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Effect of dietary soybean saponin Bb on the growth performance, intestinal nutrient absorption, morphology, microbiota, and immune response in juvenile Chinese soft-shelled turtle (Pelodiscus sinensis)

Soybean meal is widely applied in the aquafeeds due to the limitation of fish meal resources. Numerous studies have manifested that dietary soybean saponin, an anti-nutrient factor in soybean meal, may slow growth and induce intestinal inflammation in aquatic animals, but the possible causes are unc...

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Autores principales: Wang, Yue, Jia, Xinyue, Guo, Zixue, Li, Ling, Liu, Tianyu, Zhang, Peiyu, Liu, Haiyan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9816404/
https://www.ncbi.nlm.nih.gov/pubmed/36618377
http://dx.doi.org/10.3389/fimmu.2022.1093567
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author Wang, Yue
Jia, Xinyue
Guo, Zixue
Li, Ling
Liu, Tianyu
Zhang, Peiyu
Liu, Haiyan
author_facet Wang, Yue
Jia, Xinyue
Guo, Zixue
Li, Ling
Liu, Tianyu
Zhang, Peiyu
Liu, Haiyan
author_sort Wang, Yue
collection PubMed
description Soybean meal is widely applied in the aquafeeds due to the limitation of fish meal resources. Numerous studies have manifested that dietary soybean saponin, an anti-nutrient factor in soybean meal, may slow growth and induce intestinal inflammation in aquatic animals, but the possible causes are unclear. The juvenile Pelodiscus sinensis (mean initial body weight: 6.92 ± 0.03 g) were fed basal diet (CON group) and 2.46% soybean saponin Bb-supplemented diet (SAP group) for 35 days to further explore the effects of dietary soybean saponin Bb on the growth performance, apparent digestibility coefficients, intestinal morphology, the gut microbiota, intestinal transporters/channels, and immune-related gene expression. The results indicated that dietary soybean saponin Bb significantly decreased final body weight, specific growth rate, protein deposition ratio, and apparent digestibility coefficients (dry matter, crude protein, and crude lipid) of nutrients in Pelodiscus sinensis, which may be closely correlated with markedly atrophic villus height and increased lamina propria width in the small intestine. In addition, plasma contents of cholesterol, calcium, phosphorus, potassium, lysozyme, and C3 were significantly decreased in the SAP group compared with the control group. Soybean saponin Bb significantly downregulated the mRNA levels of glucose transporter 2, fatty acid binding protein 1 and fatty acid binding protein 2, amino acid transporter 2, b(0,+)-type amino acid transporter 1, and sodium-dependent phosphate transport protein 2b in the small intestine. At the same time, the expressions of key transcription factors (STAT1, TBX21, FOS), chemokines (CCL3), cytokines (TNF-α, IL-8), and aquaporins (AQP3, AQP6) in the inflammatory response were increased by soybean saponin Bb in the large intestine of a turtle. Additionally, dietary supplementation of SAP significantly reduced the generic abundance of beneficial bacteria (Lactobacillus, Bifidobacterium, and Bacillus) and harmful bacteria (Helicobacter and Bacteroides). In a nutshell, dietary supplementation of 2.46% soybean saponin not only hindered the growth performance by negatively affecting the macronutrients absorption in the small intestine but also induced an inflammatory response in the large intestine possibly by damaging the intestinal morphology, disturbing the intestinal microbiota and decreasing intestinal epithelial cell membrane permeability.
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spelling pubmed-98164042023-01-07 Effect of dietary soybean saponin Bb on the growth performance, intestinal nutrient absorption, morphology, microbiota, and immune response in juvenile Chinese soft-shelled turtle (Pelodiscus sinensis) Wang, Yue Jia, Xinyue Guo, Zixue Li, Ling Liu, Tianyu Zhang, Peiyu Liu, Haiyan Front Immunol Immunology Soybean meal is widely applied in the aquafeeds due to the limitation of fish meal resources. Numerous studies have manifested that dietary soybean saponin, an anti-nutrient factor in soybean meal, may slow growth and induce intestinal inflammation in aquatic animals, but the possible causes are unclear. The juvenile Pelodiscus sinensis (mean initial body weight: 6.92 ± 0.03 g) were fed basal diet (CON group) and 2.46% soybean saponin Bb-supplemented diet (SAP group) for 35 days to further explore the effects of dietary soybean saponin Bb on the growth performance, apparent digestibility coefficients, intestinal morphology, the gut microbiota, intestinal transporters/channels, and immune-related gene expression. The results indicated that dietary soybean saponin Bb significantly decreased final body weight, specific growth rate, protein deposition ratio, and apparent digestibility coefficients (dry matter, crude protein, and crude lipid) of nutrients in Pelodiscus sinensis, which may be closely correlated with markedly atrophic villus height and increased lamina propria width in the small intestine. In addition, plasma contents of cholesterol, calcium, phosphorus, potassium, lysozyme, and C3 were significantly decreased in the SAP group compared with the control group. Soybean saponin Bb significantly downregulated the mRNA levels of glucose transporter 2, fatty acid binding protein 1 and fatty acid binding protein 2, amino acid transporter 2, b(0,+)-type amino acid transporter 1, and sodium-dependent phosphate transport protein 2b in the small intestine. At the same time, the expressions of key transcription factors (STAT1, TBX21, FOS), chemokines (CCL3), cytokines (TNF-α, IL-8), and aquaporins (AQP3, AQP6) in the inflammatory response were increased by soybean saponin Bb in the large intestine of a turtle. Additionally, dietary supplementation of SAP significantly reduced the generic abundance of beneficial bacteria (Lactobacillus, Bifidobacterium, and Bacillus) and harmful bacteria (Helicobacter and Bacteroides). In a nutshell, dietary supplementation of 2.46% soybean saponin not only hindered the growth performance by negatively affecting the macronutrients absorption in the small intestine but also induced an inflammatory response in the large intestine possibly by damaging the intestinal morphology, disturbing the intestinal microbiota and decreasing intestinal epithelial cell membrane permeability. Frontiers Media S.A. 2022-12-23 /pmc/articles/PMC9816404/ /pubmed/36618377 http://dx.doi.org/10.3389/fimmu.2022.1093567 Text en Copyright © 2022 Wang, Jia, Guo, Li, Liu, Zhang and Liu https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Wang, Yue
Jia, Xinyue
Guo, Zixue
Li, Ling
Liu, Tianyu
Zhang, Peiyu
Liu, Haiyan
Effect of dietary soybean saponin Bb on the growth performance, intestinal nutrient absorption, morphology, microbiota, and immune response in juvenile Chinese soft-shelled turtle (Pelodiscus sinensis)
title Effect of dietary soybean saponin Bb on the growth performance, intestinal nutrient absorption, morphology, microbiota, and immune response in juvenile Chinese soft-shelled turtle (Pelodiscus sinensis)
title_full Effect of dietary soybean saponin Bb on the growth performance, intestinal nutrient absorption, morphology, microbiota, and immune response in juvenile Chinese soft-shelled turtle (Pelodiscus sinensis)
title_fullStr Effect of dietary soybean saponin Bb on the growth performance, intestinal nutrient absorption, morphology, microbiota, and immune response in juvenile Chinese soft-shelled turtle (Pelodiscus sinensis)
title_full_unstemmed Effect of dietary soybean saponin Bb on the growth performance, intestinal nutrient absorption, morphology, microbiota, and immune response in juvenile Chinese soft-shelled turtle (Pelodiscus sinensis)
title_short Effect of dietary soybean saponin Bb on the growth performance, intestinal nutrient absorption, morphology, microbiota, and immune response in juvenile Chinese soft-shelled turtle (Pelodiscus sinensis)
title_sort effect of dietary soybean saponin bb on the growth performance, intestinal nutrient absorption, morphology, microbiota, and immune response in juvenile chinese soft-shelled turtle (pelodiscus sinensis)
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9816404/
https://www.ncbi.nlm.nih.gov/pubmed/36618377
http://dx.doi.org/10.3389/fimmu.2022.1093567
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