Nutrient Digestibility, Growth, Mucosal Barrier Status, and Activity of Leucocytes From Head Kidney of Atlantic Salmon Fed Marine- or Plant-Derived Protein and Lipid Sources

Nutrient digestibility, growth, and mucosal barrier status of fish skin, gills, and distal intestine were studied in Atlantic salmon fed feeds based on marine or plant-derived ingredients. The barrier status was assessed by considering the expression of four mucin genes, five genes that encode antim...

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Main Authors: Solveig L. Sørensen, Youngjin Park, Yangyang Gong, Ghana K. Vasanth, Dalia Dahle, Kjetil Korsnes, Tran Ha Phuong, Viswanath Kiron, Sjur Øyen, Karin Pittman, Mette Sørensen
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-02-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2020.623726/full
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spelling doaj-72312c3331994444b7ec4d089d84d9f22021-02-19T14:32:55ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-02-011110.3389/fimmu.2020.623726623726Nutrient Digestibility, Growth, Mucosal Barrier Status, and Activity of Leucocytes From Head Kidney of Atlantic Salmon Fed Marine- or Plant-Derived Protein and Lipid SourcesSolveig L. Sørensen0Youngjin Park1Yangyang Gong2Yangyang Gong3Ghana K. Vasanth4Dalia Dahle5Kjetil Korsnes6Kjetil Korsnes7Tran Ha Phuong8Viswanath Kiron9Sjur Øyen10Karin Pittman11Karin Pittman12Mette Sørensen13Faculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayKey Laboratory of East China Sea Fishery Resources Exploitation, Ministry of Agriculture, East China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Shanghai, ChinaFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayBioVivo Technologies AS, Bodø, NorwayFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayDepartment of Biosciences, University of Bergen, Bergen, NorwayDepartment of Biosciences, University of Bergen, Bergen, NorwayQuantidoc AS, Bergen, NorwayFaculty of Biosciences and Aquaculture, Nord University, Bodø, NorwayNutrient digestibility, growth, and mucosal barrier status of fish skin, gills, and distal intestine were studied in Atlantic salmon fed feeds based on marine or plant-derived ingredients. The barrier status was assessed by considering the expression of four mucin genes, five genes that encode antimicrobial proteins, distal intestine micromorphology, and design-based stereology of the midgut epithelium. In addition, the head kidney leukocytes were examined using flow cytometry; to understand the differences in their counts and function. Five experimental feeds containing the main components i) fishmeal and fish oil (BG1), ii) soybean meal (BG2; to induce enteritis), iii) fishmeal as the main protein source and rapeseed oil as the main lipid source (BG3), iv) a mix of plant protein concentrates as the protein sources and fish oil as the lipid source (BG4), and v) plant and marine ingredients in the ratio 70:30 (BG5) were produced for the study. Atlantic salmon with initial weight 72.7 ± 1.2 g was offered the experimental feeds for 65 days. The results revealed that the weights of all fish groups doubled, except for fish fed BG2. Fish fed the BG2 diet had lower blood cholesterol concentration, developed enteritis, had lower expression of muc2 in the distal intestine, and had a compromised barrier status in the intestine. Expression of both the mucin genes and genes that encode antimicrobial peptides were tissue-specific and some were significantly affected by diet. The fish fed BG1 and BG3 had more head kidney lymphocyte-like cells compared to BG5-fed fish, and the phagocytic activity of macrophage-like cells from the head kidney was the highest in fish fed BG1. The intestinal micromorphology and the mucosal mapping suggest two different ways by which plant-based diets can alter the gut barrier status; by either reducing the mucous cell sizes, volumetric densities and barrier status (as noted for BG2) or increasing volumetric density of mucous cells (as observed for BG4 and BG5). The results of the compromised intestinal barrier in fish fed plant ingredients should be further confirmed through transcriptomic and immunohistochemical studies to refine ingredient composition for sustainable and acceptable healthy diets.https://www.frontiersin.org/articles/10.3389/fimmu.2020.623726/fullAtlantic salmonenteritismucosal barrier statusplant ingredientsmucin geneantimicrobial genes
collection DOAJ
language English
format Article
sources DOAJ
author Solveig L. Sørensen
Youngjin Park
Yangyang Gong
Yangyang Gong
Ghana K. Vasanth
Dalia Dahle
Kjetil Korsnes
Kjetil Korsnes
Tran Ha Phuong
Viswanath Kiron
Sjur Øyen
Karin Pittman
Karin Pittman
Mette Sørensen
spellingShingle Solveig L. Sørensen
Youngjin Park
Yangyang Gong
Yangyang Gong
Ghana K. Vasanth
Dalia Dahle
Kjetil Korsnes
Kjetil Korsnes
Tran Ha Phuong
Viswanath Kiron
Sjur Øyen
Karin Pittman
Karin Pittman
Mette Sørensen
Nutrient Digestibility, Growth, Mucosal Barrier Status, and Activity of Leucocytes From Head Kidney of Atlantic Salmon Fed Marine- or Plant-Derived Protein and Lipid Sources
Frontiers in Immunology
Atlantic salmon
enteritis
mucosal barrier status
plant ingredients
mucin gene
antimicrobial genes
author_facet Solveig L. Sørensen
Youngjin Park
Yangyang Gong
Yangyang Gong
Ghana K. Vasanth
Dalia Dahle
Kjetil Korsnes
Kjetil Korsnes
Tran Ha Phuong
Viswanath Kiron
Sjur Øyen
Karin Pittman
Karin Pittman
Mette Sørensen
author_sort Solveig L. Sørensen
title Nutrient Digestibility, Growth, Mucosal Barrier Status, and Activity of Leucocytes From Head Kidney of Atlantic Salmon Fed Marine- or Plant-Derived Protein and Lipid Sources
title_short Nutrient Digestibility, Growth, Mucosal Barrier Status, and Activity of Leucocytes From Head Kidney of Atlantic Salmon Fed Marine- or Plant-Derived Protein and Lipid Sources
title_full Nutrient Digestibility, Growth, Mucosal Barrier Status, and Activity of Leucocytes From Head Kidney of Atlantic Salmon Fed Marine- or Plant-Derived Protein and Lipid Sources
title_fullStr Nutrient Digestibility, Growth, Mucosal Barrier Status, and Activity of Leucocytes From Head Kidney of Atlantic Salmon Fed Marine- or Plant-Derived Protein and Lipid Sources
title_full_unstemmed Nutrient Digestibility, Growth, Mucosal Barrier Status, and Activity of Leucocytes From Head Kidney of Atlantic Salmon Fed Marine- or Plant-Derived Protein and Lipid Sources
title_sort nutrient digestibility, growth, mucosal barrier status, and activity of leucocytes from head kidney of atlantic salmon fed marine- or plant-derived protein and lipid sources
publisher Frontiers Media S.A.
series Frontiers in Immunology
issn 1664-3224
publishDate 2021-02-01
description Nutrient digestibility, growth, and mucosal barrier status of fish skin, gills, and distal intestine were studied in Atlantic salmon fed feeds based on marine or plant-derived ingredients. The barrier status was assessed by considering the expression of four mucin genes, five genes that encode antimicrobial proteins, distal intestine micromorphology, and design-based stereology of the midgut epithelium. In addition, the head kidney leukocytes were examined using flow cytometry; to understand the differences in their counts and function. Five experimental feeds containing the main components i) fishmeal and fish oil (BG1), ii) soybean meal (BG2; to induce enteritis), iii) fishmeal as the main protein source and rapeseed oil as the main lipid source (BG3), iv) a mix of plant protein concentrates as the protein sources and fish oil as the lipid source (BG4), and v) plant and marine ingredients in the ratio 70:30 (BG5) were produced for the study. Atlantic salmon with initial weight 72.7 ± 1.2 g was offered the experimental feeds for 65 days. The results revealed that the weights of all fish groups doubled, except for fish fed BG2. Fish fed the BG2 diet had lower blood cholesterol concentration, developed enteritis, had lower expression of muc2 in the distal intestine, and had a compromised barrier status in the intestine. Expression of both the mucin genes and genes that encode antimicrobial peptides were tissue-specific and some were significantly affected by diet. The fish fed BG1 and BG3 had more head kidney lymphocyte-like cells compared to BG5-fed fish, and the phagocytic activity of macrophage-like cells from the head kidney was the highest in fish fed BG1. The intestinal micromorphology and the mucosal mapping suggest two different ways by which plant-based diets can alter the gut barrier status; by either reducing the mucous cell sizes, volumetric densities and barrier status (as noted for BG2) or increasing volumetric density of mucous cells (as observed for BG4 and BG5). The results of the compromised intestinal barrier in fish fed plant ingredients should be further confirmed through transcriptomic and immunohistochemical studies to refine ingredient composition for sustainable and acceptable healthy diets.
topic Atlantic salmon
enteritis
mucosal barrier status
plant ingredients
mucin gene
antimicrobial genes
url https://www.frontiersin.org/articles/10.3389/fimmu.2020.623726/full
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