Excessive Substitution of Fish Meal with Fermented Soybean Meal Induces Oxidative Stress by Impairing Glutathione Metabolism in Largemouth Bass (<i>Micropterus salmoides</i>)

The application of fermented soybean meal (FSBM) is an effective strategy to alleviate the shortage of fish meal (FM) in aquaculture. However, an excessive substitution ratio often reduces fish growth and induces liver oxidative stress, while the mechanism remains poorly understood. Here, an 8-week...

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Main Authors: Qiang Chen, Congcong Wang, Yulong Sun, Yan Chen, Songming Chen, Tao Han, Jiteng Wang
Format: Article
Language:English
Published: MDPI AG 2023-12-01
Series:Antioxidants
Subjects:
Online Access:https://www.mdpi.com/2076-3921/12/12/2096
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author Qiang Chen
Congcong Wang
Yulong Sun
Yan Chen
Songming Chen
Tao Han
Jiteng Wang
author_facet Qiang Chen
Congcong Wang
Yulong Sun
Yan Chen
Songming Chen
Tao Han
Jiteng Wang
author_sort Qiang Chen
collection DOAJ
description The application of fermented soybean meal (FSBM) is an effective strategy to alleviate the shortage of fish meal (FM) in aquaculture. However, an excessive substitution ratio often reduces fish growth and induces liver oxidative stress, while the mechanism remains poorly understood. Here, an 8-week feeding trial was conducted in largemouth bass (initial weight: 6.82 ± 0.09 g) to establish an oxidative stress model by replacing 50% of FM with FSBM (fermented by <i>Bacillus subtilis</i>). The results showed that FSBM substitution significantly reduced the growth performance of largemouth bass, including the weight gain rate and specific growth rate. Moreover, FSBM significantly reduced the contents of essential amino acids and total free amino acids in muscle, along with the mRNA expression of amino acids and small peptide transporters. Enzyme activity detection and liver sections showed that FSBM substitution caused liver oxidative stress, indicating the successful construction of an oxidative stress model. An integrated analysis of transcriptomic and metabolomic data revealed that FSBM substitution impaired glycine, serine and threonine metabolism, as well as glutathione metabolism. In addition, the ratio of reduced glutathione (GSH) to oxidized glutathione (GSSG) was decreased in the FSBM group, which may explain the mechanism of oxidative stress caused by FSBM substitution. Considering that glycine is an important component of glutathione synthesis, key genes involved in glycine metabolism (<i>glya</i>, <i>gnmt</i> and <i>agxt</i>) and dietary glycine supplementation should be valued to improve the availability of FSBM. This study reveals for the first time the importance of non-essential amino acids in improving the utilization of plant-based protein sources and provides original insight for the optimization of aquatic feeds.
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spelling doaj.art-4d5ad7375c8b4a75bfe1eaf6f6b2a0092023-12-22T13:48:31ZengMDPI AGAntioxidants2076-39212023-12-011212209610.3390/antiox12122096Excessive Substitution of Fish Meal with Fermented Soybean Meal Induces Oxidative Stress by Impairing Glutathione Metabolism in Largemouth Bass (<i>Micropterus salmoides</i>)Qiang Chen0Congcong Wang1Yulong Sun2Yan Chen3Songming Chen4Tao Han5Jiteng Wang6Department of Aquaculture, Zhejiang Ocean University, Zhoushan 316022, ChinaDepartment of Aquaculture, Zhejiang Ocean University, Zhoushan 316022, ChinaDepartment of Aquaculture, Zhejiang Ocean University, Zhoushan 316022, ChinaZhejiang Provincial Engineering Technology Research Center of Marine Biomedical Products, School of Food and Pharmacy, Zhejiang Ocean University, Zhoushan 316022, ChinaDepartment of Aquaculture, Zhejiang Ocean University, Zhoushan 316022, ChinaDepartment of Aquaculture, Zhejiang Ocean University, Zhoushan 316022, ChinaDepartment of Aquaculture, Zhejiang Ocean University, Zhoushan 316022, ChinaThe application of fermented soybean meal (FSBM) is an effective strategy to alleviate the shortage of fish meal (FM) in aquaculture. However, an excessive substitution ratio often reduces fish growth and induces liver oxidative stress, while the mechanism remains poorly understood. Here, an 8-week feeding trial was conducted in largemouth bass (initial weight: 6.82 ± 0.09 g) to establish an oxidative stress model by replacing 50% of FM with FSBM (fermented by <i>Bacillus subtilis</i>). The results showed that FSBM substitution significantly reduced the growth performance of largemouth bass, including the weight gain rate and specific growth rate. Moreover, FSBM significantly reduced the contents of essential amino acids and total free amino acids in muscle, along with the mRNA expression of amino acids and small peptide transporters. Enzyme activity detection and liver sections showed that FSBM substitution caused liver oxidative stress, indicating the successful construction of an oxidative stress model. An integrated analysis of transcriptomic and metabolomic data revealed that FSBM substitution impaired glycine, serine and threonine metabolism, as well as glutathione metabolism. In addition, the ratio of reduced glutathione (GSH) to oxidized glutathione (GSSG) was decreased in the FSBM group, which may explain the mechanism of oxidative stress caused by FSBM substitution. Considering that glycine is an important component of glutathione synthesis, key genes involved in glycine metabolism (<i>glya</i>, <i>gnmt</i> and <i>agxt</i>) and dietary glycine supplementation should be valued to improve the availability of FSBM. This study reveals for the first time the importance of non-essential amino acids in improving the utilization of plant-based protein sources and provides original insight for the optimization of aquatic feeds.https://www.mdpi.com/2076-3921/12/12/2096fermented soybean mealglycineglutathione metabolism<i>Micropterus salmoides</i>oxidative stress
spellingShingle Qiang Chen
Congcong Wang
Yulong Sun
Yan Chen
Songming Chen
Tao Han
Jiteng Wang
Excessive Substitution of Fish Meal with Fermented Soybean Meal Induces Oxidative Stress by Impairing Glutathione Metabolism in Largemouth Bass (<i>Micropterus salmoides</i>)
Antioxidants
fermented soybean meal
glycine
glutathione metabolism
<i>Micropterus salmoides</i>
oxidative stress
title Excessive Substitution of Fish Meal with Fermented Soybean Meal Induces Oxidative Stress by Impairing Glutathione Metabolism in Largemouth Bass (<i>Micropterus salmoides</i>)
title_full Excessive Substitution of Fish Meal with Fermented Soybean Meal Induces Oxidative Stress by Impairing Glutathione Metabolism in Largemouth Bass (<i>Micropterus salmoides</i>)
title_fullStr Excessive Substitution of Fish Meal with Fermented Soybean Meal Induces Oxidative Stress by Impairing Glutathione Metabolism in Largemouth Bass (<i>Micropterus salmoides</i>)
title_full_unstemmed Excessive Substitution of Fish Meal with Fermented Soybean Meal Induces Oxidative Stress by Impairing Glutathione Metabolism in Largemouth Bass (<i>Micropterus salmoides</i>)
title_short Excessive Substitution of Fish Meal with Fermented Soybean Meal Induces Oxidative Stress by Impairing Glutathione Metabolism in Largemouth Bass (<i>Micropterus salmoides</i>)
title_sort excessive substitution of fish meal with fermented soybean meal induces oxidative stress by impairing glutathione metabolism in largemouth bass i micropterus salmoides i
topic fermented soybean meal
glycine
glutathione metabolism
<i>Micropterus salmoides</i>
oxidative stress
url https://www.mdpi.com/2076-3921/12/12/2096
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