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Short-Term Alternate Feeding between Terrestrially Sourced Oil- and Fish Oil-Based Diets Modulates the Intestinal Microecology of Juvenile Turbot

SIMPLE SUMMARY: There have been reports on alternate feeding between diets based on different lipid sources, but how the intestinal microbiota of fish responds to alternate feeding strategies and its relevant roles in the host’s health have not been reported. The present study provides novel results...

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Autores principales: Ma, Xiuhua, Kong, Yaoyao, Xu, Houguo, Bi, Qingzhu, Liang, Mengqing, Mai, Kangsen, Zhang, Yanjiao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10215124/
https://www.ncbi.nlm.nih.gov/pubmed/37237464
http://dx.doi.org/10.3390/biology12050650
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author Ma, Xiuhua
Kong, Yaoyao
Xu, Houguo
Bi, Qingzhu
Liang, Mengqing
Mai, Kangsen
Zhang, Yanjiao
author_facet Ma, Xiuhua
Kong, Yaoyao
Xu, Houguo
Bi, Qingzhu
Liang, Mengqing
Mai, Kangsen
Zhang, Yanjiao
author_sort Ma, Xiuhua
collection PubMed
description SIMPLE SUMMARY: There have been reports on alternate feeding between diets based on different lipid sources, but how the intestinal microbiota of fish responds to alternate feeding strategies and its relevant roles in the host’s health have not been reported. The present study provides novel results in this area. The main objective of the study was to assess how the intestinal microbiota of fish responds to alternate feeding between diets based on different lipid sources. Foremost, the juvenile turbot accepted alternate feeding between diets based on different lipid sources with no negative effects on survival or growth performance. Additionally, novel results were observed regarding the different bacterial compositions, microbial co-occurrence networks, and functional predictions among the different alternating feeding strategies. The results of this study indicate that a more comprehensive evaluation should be conducted from the perspective of intestinal microorganisms when a new feeding strategy is applied in aquaculture practices. These results will contribute to the nutritional regulation of aquatic animals from the perspective of microorganisms. ABSTRACT: A nine-week feeding trial was conducted to investigate changes in the intestinal microbiota of turbot in response to alternate feeding between terrestrially sourced oil (TSO)- and fish oil (FO)-based diets. The following three feeding strategies were designed: (1) continuous feeding with the FO-based diet (FO group); (2) weekly alternate feeding between soybean oil (SO)- and FO-based diets (SO/FO group); and (3) weekly alternate feeding between beef tallow (BT)- and FO-based diets (BT/FO group). An intestinal bacterial community analysis showed that alternate feeding reshaped the intestinal microbial composition. Higher species richness and diversity of the intestinal microbiota were observed in the alternate-feeding groups. A PCoA analysis showed that the samples clustered separately according to the feeding strategy, and among the three groups, the SO/FO group clustered relatively closer to the BT/FO group. The alternate feeding significantly decreased the abundance of Mycoplasma and selectively enriched specific microorganisms, including short-chain fatty acid (SCFA)-producing bacteria, digestive bacteria (Corynebacterium and Sphingomonas), and several potential pathogens (Desulfovibrio and Mycobacterium). Alternate feeding may maintain the intestinal microbiota balance by improving the connectivity of the ecological network and increasing the competitive interactions within the ecological network. The alternate feeding significantly upregulated the KEGG pathways of fatty acid and lipid metabolism, glycan biosynthesis, and amino acid metabolism in the intestinal microbiota. Meanwhile, the upregulation of the KEGG pathway of lipopolysaccharide biosynthesis indicates a potential risk for intestinal health. In conclusion, short-term alternate feeding between dietary lipid sources reshapes the intestinal microecology of the juvenile turbot, possibly resulting in both positive and negative effects.
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spelling pubmed-102151242023-05-27 Short-Term Alternate Feeding between Terrestrially Sourced Oil- and Fish Oil-Based Diets Modulates the Intestinal Microecology of Juvenile Turbot Ma, Xiuhua Kong, Yaoyao Xu, Houguo Bi, Qingzhu Liang, Mengqing Mai, Kangsen Zhang, Yanjiao Biology (Basel) Article SIMPLE SUMMARY: There have been reports on alternate feeding between diets based on different lipid sources, but how the intestinal microbiota of fish responds to alternate feeding strategies and its relevant roles in the host’s health have not been reported. The present study provides novel results in this area. The main objective of the study was to assess how the intestinal microbiota of fish responds to alternate feeding between diets based on different lipid sources. Foremost, the juvenile turbot accepted alternate feeding between diets based on different lipid sources with no negative effects on survival or growth performance. Additionally, novel results were observed regarding the different bacterial compositions, microbial co-occurrence networks, and functional predictions among the different alternating feeding strategies. The results of this study indicate that a more comprehensive evaluation should be conducted from the perspective of intestinal microorganisms when a new feeding strategy is applied in aquaculture practices. These results will contribute to the nutritional regulation of aquatic animals from the perspective of microorganisms. ABSTRACT: A nine-week feeding trial was conducted to investigate changes in the intestinal microbiota of turbot in response to alternate feeding between terrestrially sourced oil (TSO)- and fish oil (FO)-based diets. The following three feeding strategies were designed: (1) continuous feeding with the FO-based diet (FO group); (2) weekly alternate feeding between soybean oil (SO)- and FO-based diets (SO/FO group); and (3) weekly alternate feeding between beef tallow (BT)- and FO-based diets (BT/FO group). An intestinal bacterial community analysis showed that alternate feeding reshaped the intestinal microbial composition. Higher species richness and diversity of the intestinal microbiota were observed in the alternate-feeding groups. A PCoA analysis showed that the samples clustered separately according to the feeding strategy, and among the three groups, the SO/FO group clustered relatively closer to the BT/FO group. The alternate feeding significantly decreased the abundance of Mycoplasma and selectively enriched specific microorganisms, including short-chain fatty acid (SCFA)-producing bacteria, digestive bacteria (Corynebacterium and Sphingomonas), and several potential pathogens (Desulfovibrio and Mycobacterium). Alternate feeding may maintain the intestinal microbiota balance by improving the connectivity of the ecological network and increasing the competitive interactions within the ecological network. The alternate feeding significantly upregulated the KEGG pathways of fatty acid and lipid metabolism, glycan biosynthesis, and amino acid metabolism in the intestinal microbiota. Meanwhile, the upregulation of the KEGG pathway of lipopolysaccharide biosynthesis indicates a potential risk for intestinal health. In conclusion, short-term alternate feeding between dietary lipid sources reshapes the intestinal microecology of the juvenile turbot, possibly resulting in both positive and negative effects. MDPI 2023-04-26 /pmc/articles/PMC10215124/ /pubmed/37237464 http://dx.doi.org/10.3390/biology12050650 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/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/).
spellingShingle Article
Ma, Xiuhua
Kong, Yaoyao
Xu, Houguo
Bi, Qingzhu
Liang, Mengqing
Mai, Kangsen
Zhang, Yanjiao
Short-Term Alternate Feeding between Terrestrially Sourced Oil- and Fish Oil-Based Diets Modulates the Intestinal Microecology of Juvenile Turbot
title Short-Term Alternate Feeding between Terrestrially Sourced Oil- and Fish Oil-Based Diets Modulates the Intestinal Microecology of Juvenile Turbot
title_full Short-Term Alternate Feeding between Terrestrially Sourced Oil- and Fish Oil-Based Diets Modulates the Intestinal Microecology of Juvenile Turbot
title_fullStr Short-Term Alternate Feeding between Terrestrially Sourced Oil- and Fish Oil-Based Diets Modulates the Intestinal Microecology of Juvenile Turbot
title_full_unstemmed Short-Term Alternate Feeding between Terrestrially Sourced Oil- and Fish Oil-Based Diets Modulates the Intestinal Microecology of Juvenile Turbot
title_short Short-Term Alternate Feeding between Terrestrially Sourced Oil- and Fish Oil-Based Diets Modulates the Intestinal Microecology of Juvenile Turbot
title_sort short-term alternate feeding between terrestrially sourced oil- and fish oil-based diets modulates the intestinal microecology of juvenile turbot
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10215124/
https://www.ncbi.nlm.nih.gov/pubmed/37237464
http://dx.doi.org/10.3390/biology12050650
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