Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon

Abstract Background The potential for alternative plant protein sources to replace limited marine ingredients in fish feeds is important for the future of the fish farming industry. However, plant ingredients in fish feeds contain antinutritional factors (ANFs) that can promote gut inflammation (ent...

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Main Authors: Król, Elżbieta, Douglas, Alex, Tocher, Douglas, Crampton, Viv, Speakman, John, Secombes, Christopher, Martin, Samuel
Format: Article in Journal/Newspaper
Language:English
Published: BioMed Central Ltd. 2016
Subjects:
Online Access:http://www.biomedcentral.com/1471-2164/17/156
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spelling ftbiomed:oai:biomedcentral.com:s12864-016-2473-0 2023-05-15T15:31:27+02:00 Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon Król, Elżbieta Douglas, Alex Tocher, Douglas Crampton, Viv Speakman, John Secombes, Christopher Martin, Samuel 2016-02-29 http://www.biomedcentral.com/1471-2164/17/156 en eng BioMed Central Ltd. http://www.biomedcentral.com/1471-2164/17/156 Copyright 2016 Król et al. Soy protein concentrate Bean protein concentrate Soybean meal Antinutritional factors Gut inflammation Enteritis Whole-animal performance Microarray Gene expression Cholesterol biosynthesis pathway Research article 2016 ftbiomed 2016-03-06T01:00:57Z Abstract Background The potential for alternative plant protein sources to replace limited marine ingredients in fish feeds is important for the future of the fish farming industry. However, plant ingredients in fish feeds contain antinutritional factors (ANFs) that can promote gut inflammation (enteritis) and compromise fish health. It is unknown whether enteritis induced by plant materials with notable differences in secondary metabolism is characterised by common or distinct gene expression patterns, and how using feeds with single vs mixed plant proteins may affect the gut transcriptome and fish performance. We used Atlantic salmon parr to investigate the transcriptome responses of distal gut to varying dietary levels (0–45 %) of soy protein concentrate (SPC) and faba bean ( Vicia faba ) protein concentrate (BPC) following an 8-week feeding trial. Soybean meal (SBM) and fish meal (FM) were used as positive and negative controls for enteritis, respectively. Gene expression profiling was performed using a microarray platform developed and validated for Atlantic salmon. Results Different plant protein materials (SPC, BPC and SBM) generated substantially different gut gene expression profiles, with relatively few transcriptomic alterations (genes, pathways and GO terms) common for all plant proteins used. When SPC and BPC were simultaneously included in the diet, they induced less extensive alterations of gut transcriptome than diets with either SPC or BPC singly, probably due to reduced levels of individual ANFs. The mixed plant protein diets were also associated with improved body composition of fish relative to the single plant protein diets, which may provide evidence for a link between the magnitude of changes in gut transcriptome and whole-animal performance. Conclusions Our results indicate that gut transcriptomic profiling provides a useful tool for testing the applicability of alternative protein sources for aquaculture feeds and designing diets with reduced impact of ANFs on fish health. Ultimately, understanding diet-gut interactions and intestinal homeostasis in farmed fish is important to maximise performance and to ensure that aquaculture continues to be a sustainable source of food for a growing world population. Article in Journal/Newspaper Atlantic salmon BioMed Central
institution Open Polar
collection BioMed Central
op_collection_id ftbiomed
language English
topic Soy protein concentrate
Bean protein concentrate
Soybean meal
Antinutritional factors
Gut inflammation
Enteritis
Whole-animal performance
Microarray
Gene expression
Cholesterol biosynthesis pathway
spellingShingle Soy protein concentrate
Bean protein concentrate
Soybean meal
Antinutritional factors
Gut inflammation
Enteritis
Whole-animal performance
Microarray
Gene expression
Cholesterol biosynthesis pathway
Król, Elżbieta
Douglas, Alex
Tocher, Douglas
Crampton, Viv
Speakman, John
Secombes, Christopher
Martin, Samuel
Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon
topic_facet Soy protein concentrate
Bean protein concentrate
Soybean meal
Antinutritional factors
Gut inflammation
Enteritis
Whole-animal performance
Microarray
Gene expression
Cholesterol biosynthesis pathway
description Abstract Background The potential for alternative plant protein sources to replace limited marine ingredients in fish feeds is important for the future of the fish farming industry. However, plant ingredients in fish feeds contain antinutritional factors (ANFs) that can promote gut inflammation (enteritis) and compromise fish health. It is unknown whether enteritis induced by plant materials with notable differences in secondary metabolism is characterised by common or distinct gene expression patterns, and how using feeds with single vs mixed plant proteins may affect the gut transcriptome and fish performance. We used Atlantic salmon parr to investigate the transcriptome responses of distal gut to varying dietary levels (0–45 %) of soy protein concentrate (SPC) and faba bean ( Vicia faba ) protein concentrate (BPC) following an 8-week feeding trial. Soybean meal (SBM) and fish meal (FM) were used as positive and negative controls for enteritis, respectively. Gene expression profiling was performed using a microarray platform developed and validated for Atlantic salmon. Results Different plant protein materials (SPC, BPC and SBM) generated substantially different gut gene expression profiles, with relatively few transcriptomic alterations (genes, pathways and GO terms) common for all plant proteins used. When SPC and BPC were simultaneously included in the diet, they induced less extensive alterations of gut transcriptome than diets with either SPC or BPC singly, probably due to reduced levels of individual ANFs. The mixed plant protein diets were also associated with improved body composition of fish relative to the single plant protein diets, which may provide evidence for a link between the magnitude of changes in gut transcriptome and whole-animal performance. Conclusions Our results indicate that gut transcriptomic profiling provides a useful tool for testing the applicability of alternative protein sources for aquaculture feeds and designing diets with reduced impact of ANFs on fish health. Ultimately, understanding diet-gut interactions and intestinal homeostasis in farmed fish is important to maximise performance and to ensure that aquaculture continues to be a sustainable source of food for a growing world population.
format Article in Journal/Newspaper
author Król, Elżbieta
Douglas, Alex
Tocher, Douglas
Crampton, Viv
Speakman, John
Secombes, Christopher
Martin, Samuel
author_facet Król, Elżbieta
Douglas, Alex
Tocher, Douglas
Crampton, Viv
Speakman, John
Secombes, Christopher
Martin, Samuel
author_sort Król, Elżbieta
title Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon
title_short Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon
title_full Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon
title_fullStr Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon
title_full_unstemmed Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon
title_sort differential responses of the gut transcriptome to plant protein diets in farmed atlantic salmon
publisher BioMed Central Ltd.
publishDate 2016
url http://www.biomedcentral.com/1471-2164/17/156
genre Atlantic salmon
genre_facet Atlantic salmon
op_relation http://www.biomedcentral.com/1471-2164/17/156
op_rights Copyright 2016 Król et al.
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