Effects of fermented soybean meal substitution for fish meal on intestinal flora and intestinal health in pearl gentian grouper

This study explored the role of replacing fish meal protein with fermented soybean meal (FSBM) protein on the growth performance and intestinal morphology, immunity, and microbiota of the pearl gentian grouper (Epinephelus fuscoguttatus♀ × E. lanceolatus♂). Three isonitrogenous and isolipidic diets...

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Main Authors: Aobo Pang, Cong Peng, Ruitao Xie, Zhuoduo Wang, Beiping Tan, Tingting Wang, Wei Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-07-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2023.1194071/full
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author Aobo Pang
Aobo Pang
Aobo Pang
Cong Peng
Cong Peng
Cong Peng
Ruitao Xie
Zhuoduo Wang
Beiping Tan
Beiping Tan
Beiping Tan
Tingting Wang
Tingting Wang
Tingting Wang
Wei Zhang
Wei Zhang
Wei Zhang
author_facet Aobo Pang
Aobo Pang
Aobo Pang
Cong Peng
Cong Peng
Cong Peng
Ruitao Xie
Zhuoduo Wang
Beiping Tan
Beiping Tan
Beiping Tan
Tingting Wang
Tingting Wang
Tingting Wang
Wei Zhang
Wei Zhang
Wei Zhang
author_sort Aobo Pang
collection DOAJ
description This study explored the role of replacing fish meal protein with fermented soybean meal (FSBM) protein on the growth performance and intestinal morphology, immunity, and microbiota of the pearl gentian grouper (Epinephelus fuscoguttatus♀ × E. lanceolatus♂). Three isonitrogenous and isolipidic diets with increasing levels of FSBM (0%, 20% and 40%; referred to as FM, FSBM20 and FSBM40 diets, respectively) as a replacement for fish meal were selected for this study. The pearl gentian grouper were fed these diets for 10 weeks. The findings revealed that the growth of fish fed the FSBM diets (FSBM20 and FSBM40) were remarkably lower than the fish fed the FM diet. Pathological manifestations of intestinal inflammation, such as shortened intestinal mucosal folds and thickened lamina propria, were observed in the fish fed the FSBM diets. Moreover, the gene expression levels of IL1β, IL12, IL17, and TNFα were remarkably upregulated in fish fed the FSBM40 diet, in contrast to the gene expression levels of IL4, IL5, IL10, and TGFβ1, which were remarkably downregulated (p < 0.05). The FSBM diets significantly affected the stability of the fish gut microbiota. Photobacterium was the dominant phylum in all experimental groups, and the proportion of these bacteria gradually decreased with increasing FSBM substitution. The composition of intestinal flora at the genus level was not the same in the three experimental groups, with a richer composition of intestinal bacteria detected in the FSBM20 and FSBM40 groups (p < 0.05). The correlation between intestinal flora balance and immune gene expression revealed that only Photobacterium was negatively correlated with the above upregulated genes, while other bacteria were positively correlated with these pro-inflammatory factors (p < 0.05). Photobacterium was positively correlated with the above downregulated genes, while other bacteria were negatively correlated with these anti-inflammatory factors (p < 0.05). In conclusion, high levels of substitution of FSBM for fish meal causes intestinal inflammation in pearl gentian grouper. This is likely associated with changes to the intestinal flora. More attention should be paid to the negative role of dietary FSBM on intestinal flora.
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spelling doaj.art-021a7ecec5d34ad4939f0ca216e4fcf12023-07-03T11:06:45ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2023-07-011410.3389/fphys.2023.11940711194071Effects of fermented soybean meal substitution for fish meal on intestinal flora and intestinal health in pearl gentian grouperAobo Pang0Aobo Pang1Aobo Pang2Cong Peng3Cong Peng4Cong Peng5Ruitao Xie6Zhuoduo Wang7Beiping Tan8Beiping Tan9Beiping Tan10Tingting Wang11Tingting Wang12Tingting Wang13Wei Zhang14Wei Zhang15Wei Zhang16Laboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang, Guangdong, ChinaAquatic Animals Precision Nutrition and High Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, Guangdong, ChinaKey Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, Guangdong, ChinaLaboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang, Guangdong, ChinaAquatic Animals Precision Nutrition and High Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, Guangdong, ChinaKey Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, Guangdong, ChinaGuangdong Evergreen Feed Industry Co, Ltd., Zhangjiang, ChinaGuangdong Evergreen Feed Industry Co, Ltd., Zhangjiang, ChinaLaboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang, Guangdong, ChinaAquatic Animals Precision Nutrition and High Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, Guangdong, ChinaKey Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, Guangdong, ChinaLaboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang, Guangdong, ChinaAquatic Animals Precision Nutrition and High Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, Guangdong, ChinaKey Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, Guangdong, ChinaLaboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang, Guangdong, ChinaAquatic Animals Precision Nutrition and High Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, Guangdong, ChinaKey Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, Guangdong, ChinaThis study explored the role of replacing fish meal protein with fermented soybean meal (FSBM) protein on the growth performance and intestinal morphology, immunity, and microbiota of the pearl gentian grouper (Epinephelus fuscoguttatus♀ × E. lanceolatus♂). Three isonitrogenous and isolipidic diets with increasing levels of FSBM (0%, 20% and 40%; referred to as FM, FSBM20 and FSBM40 diets, respectively) as a replacement for fish meal were selected for this study. The pearl gentian grouper were fed these diets for 10 weeks. The findings revealed that the growth of fish fed the FSBM diets (FSBM20 and FSBM40) were remarkably lower than the fish fed the FM diet. Pathological manifestations of intestinal inflammation, such as shortened intestinal mucosal folds and thickened lamina propria, were observed in the fish fed the FSBM diets. Moreover, the gene expression levels of IL1β, IL12, IL17, and TNFα were remarkably upregulated in fish fed the FSBM40 diet, in contrast to the gene expression levels of IL4, IL5, IL10, and TGFβ1, which were remarkably downregulated (p < 0.05). The FSBM diets significantly affected the stability of the fish gut microbiota. Photobacterium was the dominant phylum in all experimental groups, and the proportion of these bacteria gradually decreased with increasing FSBM substitution. The composition of intestinal flora at the genus level was not the same in the three experimental groups, with a richer composition of intestinal bacteria detected in the FSBM20 and FSBM40 groups (p < 0.05). The correlation between intestinal flora balance and immune gene expression revealed that only Photobacterium was negatively correlated with the above upregulated genes, while other bacteria were positively correlated with these pro-inflammatory factors (p < 0.05). Photobacterium was positively correlated with the above downregulated genes, while other bacteria were negatively correlated with these anti-inflammatory factors (p < 0.05). In conclusion, high levels of substitution of FSBM for fish meal causes intestinal inflammation in pearl gentian grouper. This is likely associated with changes to the intestinal flora. More attention should be paid to the negative role of dietary FSBM on intestinal flora.https://www.frontiersin.org/articles/10.3389/fphys.2023.1194071/fullfermented soybean mealgrowth performanceintestinal morphologyintestinal inflammationintestinal floraEpinephelus fuscoguttatus♀ × E. lanceolatus♂
spellingShingle Aobo Pang
Aobo Pang
Aobo Pang
Cong Peng
Cong Peng
Cong Peng
Ruitao Xie
Zhuoduo Wang
Beiping Tan
Beiping Tan
Beiping Tan
Tingting Wang
Tingting Wang
Tingting Wang
Wei Zhang
Wei Zhang
Wei Zhang
Effects of fermented soybean meal substitution for fish meal on intestinal flora and intestinal health in pearl gentian grouper
Frontiers in Physiology
fermented soybean meal
growth performance
intestinal morphology
intestinal inflammation
intestinal flora
Epinephelus fuscoguttatus♀ × E. lanceolatus♂
title Effects of fermented soybean meal substitution for fish meal on intestinal flora and intestinal health in pearl gentian grouper
title_full Effects of fermented soybean meal substitution for fish meal on intestinal flora and intestinal health in pearl gentian grouper
title_fullStr Effects of fermented soybean meal substitution for fish meal on intestinal flora and intestinal health in pearl gentian grouper
title_full_unstemmed Effects of fermented soybean meal substitution for fish meal on intestinal flora and intestinal health in pearl gentian grouper
title_short Effects of fermented soybean meal substitution for fish meal on intestinal flora and intestinal health in pearl gentian grouper
title_sort effects of fermented soybean meal substitution for fish meal on intestinal flora and intestinal health in pearl gentian grouper
topic fermented soybean meal
growth performance
intestinal morphology
intestinal inflammation
intestinal flora
Epinephelus fuscoguttatus♀ × E. lanceolatus♂
url https://www.frontiersin.org/articles/10.3389/fphys.2023.1194071/full
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