Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon
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 compromi...
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description | 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.
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.
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. |
doi_str_mv | 10.1186/s12864-016-2473-0 |
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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.
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.</description><identifier>ISSN: 1471-2164</identifier><identifier>EISSN: 1471-2164</identifier><identifier>DOI: 10.1186/s12864-016-2473-0</identifier><identifier>PMID: 26925977</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Analysis ; Animal Feed - analysis ; Animal Nutritional Physiological Phenomena ; Animals ; Aquaculture ; Atlantic salmon ; Diet ; Gene expression ; Gene Expression Profiling ; Genomics ; Glycine max - chemistry ; Health aspects ; Intestinal Mucosa - metabolism ; Phenotype ; Physiological aspects ; Plant Proteins, Dietary - chemistry ; Salmo salar - metabolism ; Transcriptome ; Vicia faba - chemistry</subject><ispartof>BMC genomics, 2016-02, Vol.17 (145), p.156, Article 156</ispartof><rights>COPYRIGHT 2016 BioMed Central Ltd.</rights><rights>Copyright BioMed Central 2016</rights><rights>Król et al. 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c594t-3d2f27862e2fed47d97ce3f299432446ff39c1e6e711795fb786d908cb92acb03</citedby><cites>FETCH-LOGICAL-c594t-3d2f27862e2fed47d97ce3f299432446ff39c1e6e711795fb786d908cb92acb03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4772681/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4772681/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27923,27924,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26925977$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Król, Elżbieta</creatorcontrib><creatorcontrib>Douglas, Alex</creatorcontrib><creatorcontrib>Tocher, Douglas R</creatorcontrib><creatorcontrib>Crampton, Viv O</creatorcontrib><creatorcontrib>Speakman, John R</creatorcontrib><creatorcontrib>Secombes, Christopher J</creatorcontrib><creatorcontrib>Martin, Samuel A M</creatorcontrib><title>Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon</title><title>BMC genomics</title><addtitle>BMC Genomics</addtitle><description>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.
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.
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.</description><subject>Analysis</subject><subject>Animal Feed - analysis</subject><subject>Animal Nutritional Physiological Phenomena</subject><subject>Animals</subject><subject>Aquaculture</subject><subject>Atlantic salmon</subject><subject>Diet</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Genomics</subject><subject>Glycine max - chemistry</subject><subject>Health aspects</subject><subject>Intestinal Mucosa - metabolism</subject><subject>Phenotype</subject><subject>Physiological aspects</subject><subject>Plant Proteins, Dietary - chemistry</subject><subject>Salmo salar - metabolism</subject><subject>Transcriptome</subject><subject>Vicia faba - chemistry</subject><issn>1471-2164</issn><issn>1471-2164</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNptUk2LFDEQDaK46-oP8CIBTx567aQzqc5FGNavhQXBj3PMpCuzWbqTNkmL_nvTzLrugOSQIvXeq1fhEfKcteeM9fJ1ZryXommZbLiArmkfkFMmgDWcSfHwXn1CnuR807YMer55TE64VHyjAE7J97feOUwYijcjTZjnGDJmGh0t10j3S6ElmZBt8nOJE9IS6TyaUOicYkEf6OCxZFoLZ9KEA92Wte0tzWacYnhKHjkzZnx2e5-Rb-_ffb342Fx9-nB5sb1q7EaJ0nQDdxx6yZE7HAQMCix2jislOi6EdK5TlqFEYAzUxu0qdlBtb3eKG7truzPy5qA7L7tqw9aNkhn1nPxk0m8djdfHneCv9T7-1AKAy55VgZe3Ain-WDAXfROXFKpnzaCOZD0A_EPtzYjaBxermJ18tnorhADeK7WaOf8Pqp4BJ29jQOfr-xHh1RGhYgr-Knuz5Kwvv3w-xrID1qaYc0J3tyRr9ZoLfciFrrnQay70ynlx_3fuGH-D0P0Bp4uzKA</recordid><startdate>20160229</startdate><enddate>20160229</enddate><creator>Król, Elżbieta</creator><creator>Douglas, Alex</creator><creator>Tocher, Douglas R</creator><creator>Crampton, Viv O</creator><creator>Speakman, John R</creator><creator>Secombes, Christopher J</creator><creator>Martin, Samuel A M</creator><general>BioMed Central Ltd</general><general>BioMed Central</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7U7</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>5PM</scope></search><sort><creationdate>20160229</creationdate><title>Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon</title><author>Król, Elżbieta ; Douglas, Alex ; Tocher, Douglas R ; Crampton, Viv O ; Speakman, John R ; Secombes, Christopher J ; Martin, Samuel A M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c594t-3d2f27862e2fed47d97ce3f299432446ff39c1e6e711795fb786d908cb92acb03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Analysis</topic><topic>Animal Feed - 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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.
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.
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.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>26925977</pmid><doi>10.1186/s12864-016-2473-0</doi><oa>free_for_read</oa></addata></record> |
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subjects | Analysis Animal Feed - analysis Animal Nutritional Physiological Phenomena Animals Aquaculture Atlantic salmon Diet Gene expression Gene Expression Profiling Genomics Glycine max - chemistry Health aspects Intestinal Mucosa - metabolism Phenotype Physiological aspects Plant Proteins, Dietary - chemistry Salmo salar - metabolism Transcriptome Vicia faba - chemistry |
title | Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon |
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