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

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)...

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Autores principales: Król, Elżbieta, Douglas, Alex, Tocher, Douglas R., Crampton, Viv O., Speakman, John R., Secombes, Christopher J., Martin, Samuel A. M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4772681/
https://www.ncbi.nlm.nih.gov/pubmed/26925977
http://dx.doi.org/10.1186/s12864-016-2473-0
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author Król, Elżbieta
Douglas, Alex
Tocher, Douglas R.
Crampton, Viv O.
Speakman, John R.
Secombes, Christopher J.
Martin, Samuel A. M.
author_facet Król, Elżbieta
Douglas, Alex
Tocher, Douglas R.
Crampton, Viv O.
Speakman, John R.
Secombes, Christopher J.
Martin, Samuel A. M.
author_sort Król, Elżbieta
collection PubMed
description 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-2473-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-47726812016-03-02 Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon Król, Elżbieta Douglas, Alex Tocher, Douglas R. Crampton, Viv O. Speakman, John R. Secombes, Christopher J. Martin, Samuel A. M. BMC Genomics Research Article 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-2473-0) contains supplementary material, which is available to authorized users. BioMed Central 2016-02-29 /pmc/articles/PMC4772681/ /pubmed/26925977 http://dx.doi.org/10.1186/s12864-016-2473-0 Text en © Król et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Król, Elżbieta
Douglas, Alex
Tocher, Douglas R.
Crampton, Viv O.
Speakman, John R.
Secombes, Christopher J.
Martin, Samuel A. M.
Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon
title 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_short 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
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4772681/
https://www.ncbi.nlm.nih.gov/pubmed/26925977
http://dx.doi.org/10.1186/s12864-016-2473-0
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