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) a...

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Published in:BMC Genomics
Main Authors: Krol, Elzbieta, Douglas, Alex, Tocher, Douglas R, Crampton, Viv O, Speakman, John R, Secombes, Christopher J, Martin, Samuel A M
Other Authors: University of Aberdeen, Institute of Aquaculture, EWOS Innovation, orcid:0000-0002-8603-9410
Format: Article in Journal/Newspaper
Language:English
Published: BioMed Central 2016
Subjects:
Online Access:http://hdl.handle.net/1893/24003
https://doi.org/10.1186/s12864-016-2473-0
http://dspace.stir.ac.uk/bitstream/1893/24003/1/Differential%20responses%20of%20the%20gut%20transcriptome.pdf
id ftunivstirling:oai:dspace.stir.ac.uk:1893/24003
record_format openpolar
institution Open Polar
collection University of Stirling: Stirling Digital Research Repository
op_collection_id ftunivstirling
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
Krol, Elzbieta
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
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 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 ...
author2 University of Aberdeen
Institute of Aquaculture
EWOS Innovation
orcid:0000-0002-8603-9410
format Article in Journal/Newspaper
author Krol, Elzbieta
Douglas, Alex
Tocher, Douglas R
Crampton, Viv O
Speakman, John R
Secombes, Christopher J
Martin, Samuel A M
author_facet Krol, Elzbieta
Douglas, Alex
Tocher, Douglas R
Crampton, Viv O
Speakman, John R
Secombes, Christopher J
Martin, Samuel A M
author_sort Krol, Elzbieta
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
publishDate 2016
url http://hdl.handle.net/1893/24003
https://doi.org/10.1186/s12864-016-2473-0
http://dspace.stir.ac.uk/bitstream/1893/24003/1/Differential%20responses%20of%20the%20gut%20transcriptome.pdf
genre Atlantic salmon
genre_facet Atlantic salmon
op_relation Krol E, Douglas A, Tocher DR, Crampton VO, Speakman JR, Secombes CJ & Martin SAM (2016) Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon. BMC Genomics, 17, Art. No.: 156. https://doi.org/10.1186/s12864-016-2473-0
156
http://hdl.handle.net/1893/24003
doi:10.1186/s12864-016-2473-0
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WOS:000371594300007
2-s2.0-84978712558
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http://dspace.stir.ac.uk/bitstream/1893/24003/1/Differential%20responses%20of%20the%20gut%20transcriptome.pdf
op_rights © Król et al. 2016 This 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.
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spelling ftunivstirling:oai:dspace.stir.ac.uk:1893/24003 2023-05-15T15:31:14+02:00 Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon Krol, Elzbieta Douglas, Alex Tocher, Douglas R Crampton, Viv O Speakman, John R Secombes, Christopher J Martin, Samuel A M University of Aberdeen Institute of Aquaculture EWOS Innovation orcid:0000-0002-8603-9410 2016-02-29 application/pdf http://hdl.handle.net/1893/24003 https://doi.org/10.1186/s12864-016-2473-0 http://dspace.stir.ac.uk/bitstream/1893/24003/1/Differential%20responses%20of%20the%20gut%20transcriptome.pdf en eng BioMed Central Krol E, Douglas A, Tocher DR, Crampton VO, Speakman JR, Secombes CJ & Martin SAM (2016) Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon. BMC Genomics, 17, Art. No.: 156. https://doi.org/10.1186/s12864-016-2473-0 156 http://hdl.handle.net/1893/24003 doi:10.1186/s12864-016-2473-0 26925977 WOS:000371594300007 2-s2.0-84978712558 553748 http://dspace.stir.ac.uk/bitstream/1893/24003/1/Differential%20responses%20of%20the%20gut%20transcriptome.pdf © Król et al. 2016 This 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. http://creativecommons.org/licenses/by/4.0/ CC0 PDM CC-BY Soy protein concentrate Bean protein concentrate Soybean meal Antinutritional factors Gut inflammation Enteritis Whole-animal performance Microarray Gene expression Cholesterol biosynthesis pathway Journal Article VoR - Version of Record 2016 ftunivstirling https://doi.org/10.1186/s12864-016-2473-0 2022-06-13T18:43:55Z 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 ... Article in Journal/Newspaper Atlantic salmon University of Stirling: Stirling Digital Research Repository BMC Genomics 17 1