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

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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.
Original languageEnglish
Article number156
Pages (from-to)1-16
Number of pages16
JournalBMC Genomics
Volume17
DOIs
Publication statusPublished - 29 Feb 2016

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Salmo salar
Plant Proteins
Transcriptome
Fishes
Vicia faba
Diet
Soybean Proteins
Enteritis
Meals
Aquaculture
Proteins
Secondary Metabolism
Health
Gene Expression Profiling
Body Composition
Agriculture
Soybeans
Industry
Homeostasis
Inflammation

Keywords

  • Soy protein concentrate
  • Bean protein concentrate
  • Soybean meal
  • Antinutritional factors
  • Gut inflammation
  • Enteritis
  • Whole-animal performance
  • Microarray
  • Gene expression
  • Cholesterol biosynthesis pathway

Cite this

@article{3b886ae955fb43f2bc6a41d6f6ee9057,
title = "Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon",
abstract = "BackgroundThe 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.ResultsDifferent 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.ConclusionsOur 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.",
keywords = "Soy protein concentrate, Bean protein concentrate, Soybean meal, Antinutritional factors, Gut inflammation, Enteritis, Whole-animal performance, Microarray , Gene expression, Cholesterol biosynthesis pathway",
author = "Elzbieta Krol and Alex Douglas and Tocher, {Douglas R.} and Crampton, {Viv O.} and Speakman, {John R.} and Secombes, {Christopher J.} and Martin, {Samuel A. M.}",
note = "Acknowledgements The study was supported by the UK Technology Strategy Board (TSB Grant 11974-81166). We are grateful to the three anonymous referees who made valuable comments on the earlier version of the manuscript.",
year = "2016",
month = "2",
day = "29",
doi = "10.1186/s12864-016-2473-0",
language = "English",
volume = "17",
pages = "1--16",
journal = "BMC Genomics",
issn = "1471-2164",
publisher = "BioMed Central",

}

TY - JOUR

T1 - Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon

AU - Krol, Elzbieta

AU - Douglas, Alex

AU - Tocher, Douglas R.

AU - Crampton, Viv O.

AU - Speakman, John R.

AU - Secombes, Christopher J.

AU - Martin, Samuel A. M.

N1 - Acknowledgements The study was supported by the UK Technology Strategy Board (TSB Grant 11974-81166). We are grateful to the three anonymous referees who made valuable comments on the earlier version of the manuscript.

PY - 2016/2/29

Y1 - 2016/2/29

N2 - BackgroundThe 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.ResultsDifferent 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.ConclusionsOur 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.

AB - BackgroundThe 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.ResultsDifferent 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.ConclusionsOur 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.

KW - Soy protein concentrate

KW - Bean protein concentrate

KW - Soybean meal

KW - Antinutritional factors

KW - Gut inflammation

KW - Enteritis

KW - Whole-animal performance

KW - Microarray

KW - Gene expression

KW - Cholesterol biosynthesis pathway

U2 - 10.1186/s12864-016-2473-0

DO - 10.1186/s12864-016-2473-0

M3 - Article

VL - 17

SP - 1

EP - 16

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

M1 - 156

ER -