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Liver Transcriptome Profiling Reveals That Dietary DHA and EPA Levels Influence Suites of Genes Involved in Metabolism, Redox Homeostasis, and Immune Function in Atlantic Salmon (Salmo salar)

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Abstract

The optimal dietary requirement of omega-3 long-chain polyunsaturated fatty acids (ω3 LC-PUFA), namely docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA), for Atlantic salmon that promotes growth and health warrants careful investigation. We used 44K microarrays to study the influence of increasing levels of dietary DHA + EPA (0, 1.0, and 1.4% of the diet, as formulated) in the presence of high linoleic acid (LA) on Atlantic salmon growth and liver transcriptome. After a 14-week feeding trial, Atlantic salmon fed diet ω3LC0 (i.e. 0% of DHA + EPA) showed significantly lower final weight and weight gain, and higher feed conversion ratio compared with ω3LC1.0 and ω3LC1.4 diet groups. The microarray experiment identified 55 and 77 differentially expressed probes (Rank Products analyses; PFP < 10%) in salmon fed diets ω3LC1.4 and ω3LC1.0 compared with those fed diet ω3LC0, respectively. The comparison between ω3LC1.4 and ω3LC1.0 revealed 134 differentially expressed probes. The microarray results were confirmed by qPCR analyses of 22 microarray-identified transcripts. Several key genes involved in fatty acid metabolism including LC-PUFA synthesis were upregulated in fish fed ω3LC0 compared with both other groups. Hierarchical clustering and linear regression analyses of liver qPCR and fatty acid composition data demonstrated significant correlations. In the current study, 1.0% ω3 LC-PUFA seemed to be the minimum requirement for Atlantic salmon based on growth performance; however, multivariate statistical analyses (PERMANOVA and SIMPER) showed that fish fed ω3LC1.0 and ω3LC1.4 diets had similar hepatic fatty acid profiles but marked differences in the transcript expression of biomarker genes involved in redox homeostasis (mgst1), immune responses (mxb, igmb, irf3, lect2a, srk2, and lyz2), and LC-PUFA synthesis (srebp1, fadsd5, and elovl2). This research has provided new insights into dietary requirement of DHA and EPA and their impact on physiologically important pathways in addition to lipid metabolism in Atlantic salmon.

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References

  • Alvarez M, Diez A, Lopez-Bote C, Gallego M, Bautista J (2000) Short-term modulation of lipogenesis by macronutrients in rainbow trout (Oncorhynchus mykiss) hepatocytes. Br J Nutr 84:619–628

    Article  CAS  PubMed  Google Scholar 

  • Bañuelos-Vargas I, López LM, Pérez-Jiménez A, Peres H (2014) Effect of fishmeal replacement by soy protein concentrate with taurine supplementation on hepatic intermediary metabolism and antioxidant status of totoaba juveniles (Totoaba macdonaldi). Comp Biochem Physiol B: Biochem Mol Biol 170:18–25

    Article  CAS  Google Scholar 

  • Beheshti Foroutani M (2017) Minimizing marine resource utilization in diets of farmed Atlantic salmon (Salmo salar): effects on growth performance and muscle, liver, and head kidney chemical composition. MSc thesis Memorial University of Newfoundland, St John’s

  • Beheshti Foroutani M, Parrish CC, Wells J, Taylor RG, Rise ML, Shahidi F (2018) Minimizing marine ingredients in diets of farmed Atlantic salmon (Salmo salar): effects on growth performance and muscle lipid and fatty acid composition. PLoS One 13:e0198538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bell JG, McEvoy J, Tocher DR, McGhee F, Campbell PJ, Sargent JR (2001) Replacement of fish oil with rapeseed oil in diets of Atlantic salmon (Salmo salar) affects tissue lipid compositions and hepatocyte fatty acid metabolism. J Nutr 131:1535–1543

    Article  CAS  PubMed  Google Scholar 

  • Bell JG, Strachan F, Good JE, Tocher DR (2006) Effect of dietary echium oil on growth, fatty acid composition and metabolism, gill prostaglandin production and macrophage activity in Atlantic cod (Gadus morhua L.). Aquac Res 37:606–617

    Article  CAS  Google Scholar 

  • Bell JG, Pratoomyot J, Strachan F, Henderson RJ, Fontanillas R, Hebard A, Guy DR, Hunter D, Tocher DR (2010) Growth, flesh adiposity and fatty acid composition of Atlantic salmon (Salmo salar) families with contrasting flesh adiposity: effects of replacement of dietary fish oil with vegetable oils. Aquaculture 306:225–232

    Article  CAS  Google Scholar 

  • Betancor MB, Howarth FJ, Glencross BD, Tocher DR (2014) Influence of dietary docosahexaenoic acid in combination with other long-chain polyunsaturated fatty acids on expression of biosynthesis genes and phospholipid fatty acid compositions in tissues of post-smolt Atlantic salmon (Salmo salar). Comp Biochem Physiol B Biochem Mol Biol 172-173:74–89

    Article  CAS  PubMed  Google Scholar 

  • Betancor MB, Almaida-Pagán P, Hernandez A, Tocher DR (2015) Effects of dietary fatty acids on mitochondrial phospholipid compositions, oxidative status and mitochondrial gene expression of zebrafish at different ages. Fish Physiol Biochem 41:1187–1204

    Article  CAS  PubMed  Google Scholar 

  • Betancor MB, Sprague M, Sayanova O, Usher S, Metochis C, Campbell PJ, Napier JA, Tocher DR (2016) Nutritional evaluation of an EPA-DHA oil from transgenic Camelina sativa in feeds for post-smolt Atlantic salmon (Salmo salar L.). PLoS One 11:e0159934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bo TH, Dysvik B, Jonassen I (2004) LSimpute: accurate estimation of missing values in microarray data with least squares methods. Nucleic Acids Res 32:e34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Booman M, Borza T, Feng CY, Hori TS, Higgins B, Culf A, Leger D, Chute IC, Belkaid A, Rise M, Gamperl AK, Hubert S, Kimball J, Ouellette RJ, Johnson SC, Bowman S, Rise ML (2011) Development and experimental validation of a 20K Atlantic cod (Gadus morhua) oligonucleotide microarray based on a collection of over 150,000 ESTs. Mar Biotechnol 13:733–750

    Article  CAS  PubMed  Google Scholar 

  • Bou M, Berge GM, Baeverfjord G, Sigholt T, Østbye T-K, Romarheim OH, Hatlen B, Leeuwis R, Venegas C, Ruyter B (2017a) Requirements of n-3 very long-chain PUFA in Atlantic salmon (Salmo salar L): effects of different dietary levels of EPA and DHA on fish performance and tissue composition and integrity. Br J Nutr 117:30–47

    Article  CAS  PubMed  Google Scholar 

  • Bou M, Berge GM, Baeverfjord G, Sigholt T, Østbye T-K, Ruyter B (2017b) Low levels of very-long-chain n-3 PUFA in Atlantic salmon (Salmo salar) diet reduce fish robustness under challenging conditions in sea cages. J Nutr Sci 6:E32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breitling R, Armengaud P, Amtmann A, Herzyk P (2004) Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 573:83–92

    Article  CAS  PubMed  Google Scholar 

  • Brown TD, Hori TS, Xue X, Ye CL, Anderson DM, Rise ML (2016) Functional genomic analysis of the impact of camelina (Camelina sativa) meal on Atlantic salmon (Salmo salar) distal intestine gene expression and physiology. Mar Biotechnol 18:418–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caballero-Solares A, Hall JR, Xue X, Eslamloo K, Taylor RG, Parrish CC, Rise ML (2017) The dietary replacement of marine ingredients by terrestrial animal and plant alternatives modulates the antiviral immune response of Atlantic salmon (Salmo salar). Fish Shellfish Immunol 64:24–38

    Article  CAS  PubMed  Google Scholar 

  • Caballero-Solares A, Xue X, Parrish CC, Foroutani MB, Taylor RG, Rise ML (2018) Changes in the liver transcriptome of farmed Atlantic salmon (Salmo salar) fed experimental diets based on terrestrial alternatives to fish meal and fish oil. BMC Genomics 19:796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calder PC (2013) N-3 fatty acids, inflammation and immunity: new mechanisms to explain old actions. Proc Nutr Soc 72:326–336

    Article  CAS  PubMed  Google Scholar 

  • Calder PC (2015) Marine omega-3 fatty acids and inflammatory processes: effects, mechanisms and clinical relevance. Biochim Biophys Acta Mol Cell Biol Lipids 1851:469–484

    Article  CAS  Google Scholar 

  • Celton M, Malpertuy A, Lelandais G, de Brevern AG (2010) Comparative analysis of missing value imputation methods to improve clustering and interpretation of microarray experiments. BMC Genomics 11:15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng CL, Huang SJ, Wu CL, Gong HY, Ken CF, Hu SY, Wu JL (2015) Transgenic expression of omega-3 PUFA synthesis genes improves zebrafish survival during Vibrio vulnificus infection. J Biomed Sci 22:103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  • Dentin R, Benhamed F, Pégorier J-P, Foufelle F, Viollet B, Vaulont S, Girard J, Postic C (2005) Polyunsaturated fatty acids suppress glycolytic and lipogenic genes through the inhibition of ChREBP nuclear protein translocation. J Clin Invest 115:2843–2854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eslamloo K, Xue X, Hall JR, Smith NC, Caballero-Solares A, Parrish CC, Taylor RG, Rise ML (2017) Transcriptome profiling of antiviral immune and dietary fatty acid dependent responses of Atlantic salmon macrophage-like cells. BMC Genomics 18:706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foroutani M, Parrish CC, Wells J, Taylor RG, Rise ML (In revision) Minimizing marine ingredients in diets of farmed Atlantic salmon (Salmo salar): effects on liver and head kidney lipid class, fatty acid and elemental composition. Fish Physiol Biochem

  • Fritsche K, Byrge M, Feng C (1999) Dietary omega-3 polyunsaturated fatty acids from fish oil reduce interleukin-12 and interferon-gamma production in mice. Immunol Lett 65:167–173

    Article  CAS  PubMed  Google Scholar 

  • Fu GH, Bai ZY, Xia JH, Liu XJ, Liu F, Wan ZY, Yue GH (2014) Characterization of the LECT2 gene and its associations with resistance to the big belly disease in Asian seabass. Fish Shellfish Immunol 37:131–138

    Article  CAS  PubMed  Google Scholar 

  • Gao F, Qu L, Yu S, Ye X, Tian Y, Zhang L, Bai J, Lu M (2012) Identification and expression analysis of three c-type lysozymes in Oreochromis aureus. Fish Shellfish Immunol 32:779–788

    Article  CAS  PubMed  Google Scholar 

  • Gladine C, Roy NC, Rigaudiere J-P, Laillet B, Da Silva G, Joly C, Pujos-Guillot E, Morio B, Feillet-Coudray C, McNabb WC (2012) Increasing intake of long-chain n-3 PUFA enhances lipoperoxidation and modulates hepatic gene expression in a dose-dependent manner. Br J Nutr 107:1254–1273

    Article  CAS  PubMed  Google Scholar 

  • Glencross BD (2009) Exploring the nutritional demand for essential fatty acids by aquaculture species. Rev Aquac 1:71–124

    Article  Google Scholar 

  • Glencross BD, Tocher DR, Matthew C, Bell JG (2014) Interactions between dietary docosahexaenoic acid and other long-chain polyunsaturated fatty acids on performance and fatty acid retention in post-smolt Atlantic salmon (Salmo salar). Fish Physiol Biochem 40:1213–1227

    CAS  PubMed  Google Scholar 

  • Hemre GI, Mommsen TP, Krogdahl A (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8:175–194

    Article  CAS  Google Scholar 

  • Hixson SM, Parrish CC, Anderson DM (2014) Full substitution of fish oil with camelina (Camelina sativa) oil, with partial substitution of fish meal with camelina meal, in diets for farmed Atlantic salmon (Salmo salar) and its effect on tissue lipids and sensory quality. Food Chem 157:51–61

    Article  CAS  PubMed  Google Scholar 

  • Hixson SM, Parrish CC, Xue X, Wells JS, Collins SA, Anderson DM, Rise ML (2017) Growth performance, tissue composition, and gene expression responses in Atlantic salmon (Salmo salar) fed varying levels of different lipid sources. Aquaculture 467:76–88

    Article  CAS  Google Scholar 

  • Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, Chory J (2006) RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22:2825–2827

    Article  CAS  PubMed  Google Scholar 

  • Hori TS, Gamperl AK, Booman M, Nash GW, Rise ML (2012) A moderate increase in ambient temperature modulates the Atlantic cod (Gadus morhua) spleen transcriptome response to intraperitoneal viral mimic injection. BMC Genomics 13:431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jalili M, Jin Y, Bones AM, Olsen Y, Vadstein O, Østensen M-A, Buonocore F, Gerdol M, Pallavicini A, Scapigliati G (2019) Dietary fatty acid source has little effect on the development of the immune system in the pyloric caeca of Atlantic salmon fry. Sci Rep 9:27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jantzen SG, Sanderson DS, von Schalburg KR, Yasuike M, Marass F, Koop BF (2011) A 44K microarray dataset of the changing transcriptome in developing Atlantic salmon (Salmo salar L.). BMC Res Notes 4:88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeffery IB, Higgins DG, Culhane AC (2006) Comparison and evaluation of methods for generating differentially expressed gene lists from microarray data. BMC Bioinf 7:359

    Article  CAS  Google Scholar 

  • Katan T, Caballero-Solares A, Taylor RG, Rise ML, Parrish CC (2019) Effect of plant-based diets with varying ratios of ω6 to ω3 fatty acids on growth performance, tissue composition, fatty acid biosynthesis and lipid-related gene expression in Atlantic salmon (Salmo salar). Comp Biochem Physiol Part D Genomics Proteomics 30:290–304

  • Leaver MJ, Bautista JM, Björnsson BT, Jönsson E, Krey G, Tocher DR, Torstensen BE (2008) Towards fish lipid nutrigenomics: current state and prospects for fin-fish aquaculture. Rev Fish Sci 16:73–94

    Article  CAS  Google Scholar 

  • Li MY, Chen J, Shi YH (2008) Molecular cloning of leucocyte cell-derived chemotaxin-2 gene in croceine croaker (Pseudosciaena crocea). Fish Shellfish Immunol 24:252–256

    Article  CAS  PubMed  Google Scholar 

  • Lillig CH, Berndt C, Holmgren A (2008) Glutaredoxin systems. Biochim Biophys Acta, Gen Subj 1780:1304–1317

    Article  CAS  Google Scholar 

  • Makesh M, Sudheesh PS, Cain KD (2015) Systemic and mucosal immune response of rainbow trout to immunization with an attenuated Flavobacterium psychrophilum vaccine strain by different routes. Fish Shellfish Immunol 44:156–163

    Article  CAS  PubMed  Google Scholar 

  • Minghetti M, Leaver MJ, Tocher DR (2011) Transcriptional control mechanisms of genes of lipid and fatty acid metabolism in the Atlantic salmon (Salmo salar L.) established cell line, SHK-1. Biochim Biophys Acta Mol Cell Biol Lipids 1811:194–202

    Article  CAS  Google Scholar 

  • Moldal T, Løkka G, Wiik-Nielsen J, Austbø L, Torstensen BE, Rosenlund G, Dale OB, Kaldhusdal M, Koppang EO (2014) Substitution of dietary fish oil with plant oils is associated with shortened mid intestinal folds in Atlantic salmon (Salmo salar). BMC Vet Res 10:60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montero D, Kalinowski T, Obach A, Robaina L, Tort L, Caballero MJ, Izquierdo MS (2003) Vegetable lipid sources for gilthead seabream (Sparus aurata): effects on fish health. Aquaculture 225:353–370

    Article  CAS  Google Scholar 

  • Montero D, Grasso V, Izquierdo M, Ganga R, Real F, Tort L, Caballero M, Acosta F (2008) Total substitution of fish oil by vegetable oils in gilthead sea bream (Sparus aurata) diets: effects on hepatic mx expression and some immune parameters. Fish Shellfish Immunol 24:147–155

    Article  CAS  PubMed  Google Scholar 

  • Montero D, Mathlouthi F, Tort L, Afonso JM, Torrecillas S, Fernández-Vaquero A, Negrin D, Izquierdo MS (2010) Replacement of dietary fish oil by vegetable oils affects humoral immunity and expression of pro-inflammatory cytokines genes in gilthead sea bream Sparus aurata. Fish Shellfish Immunol 29:1073–1081

    Article  CAS  PubMed  Google Scholar 

  • Morais S, Monroig O, Zheng X, Leaver MJ, Tocher DR (2009) Highly unsaturated fatty acid synthesis in Atlantic salmon: characterization of ELOVL5- and ELOVL2-like elongases. Mar Biotechnol 11:627–639

    Article  CAS  PubMed  Google Scholar 

  • Morais S, Pratoomyot J, Taggart JB, Bron JE, Guy DR, Bell JG, Tocher DR (2011) Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis. BMC Genomics 12:255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morais S, Taggart JB, Guy DR, Bell JG, Tocher DR (2012) Hepatic transcriptome analysis of inter-family variability in flesh n-3 long-chain polyunsaturated fatty acid content in Atlantic salmon. BMC Genomics 13:410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mourente G, Good JE, Bell JG (2005) Partial substitution of fish oil with rapeseed, linseed and olive oils in diets for European sea bass (Dicentrarchus labrax L.): effects on flesh fatty acid composition, plasma prostaglandins E2 and F2α, immune function and effectiveness of a fish oil finishing diet. Aquac Nutr 11:25–40

    Article  CAS  Google Scholar 

  • Mu C, Wang Q, Yuan Z, Zhang Z, Wang C (2012) Identification of glutaredoxin 1 and glutaredoxin 2 genes from Venerupis philippinarum and their responses to benzo [a] pyrene and bacterial challenge. Fish Shellfish Immunol 32:482–488

    Article  CAS  PubMed  Google Scholar 

  • Panserat S, Hortopan GA, Plagnes-Juan E, Kolditz C, Lansard M, Skiba-Cassy S, Esquerré D, Geurden I, Médale F, Kaushik S, Corraze G (2009) Differential gene expression after total replacement of dietary fish meal and fish oil by plant products in rainbow trout (Oncorhynchus mykiss) liver. Aquaculture 294:123–131

    Article  CAS  Google Scholar 

  • Patterson E, Wall R, Fitzgerald G, Ross R, Stanton C (2012) Health implications of high dietary omega-6 polyunsaturated fatty acids. J Nutr Metab 2012:539426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfaffl M (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenlund G, Torstensen BE, Stubhaug I, Usman N, Sissener NH (2016) Atlantic salmon require long-chain n-3 fatty acids for optimal growth throughout the seawater period. J Nutr Sci 5:e19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruyter B, Rosjo C, Einen O, Thomassen M (2000) Essential fatty acids in Atlantic salmon: effects of increasing dietary doses of n-6 and n-3 fatty acids on growth, survival and fatty acid composition of liver, blood and carcass. Aquac Nutr 6:119–127

    Article  CAS  Google Scholar 

  • Sahlmann C, Sutherland BJG, Kortner TM, Koop BF, Krogdahl Å, Bakke AM (2013) Early response of gene expression in the distal intestine of Atlantic salmon (Salmo salar L.) during the development of soybean meal induced enteritis. Fish Shellfish Immunol 34:599–609

    Article  CAS  PubMed  Google Scholar 

  • Salze GP, Davis DA (2015) Taurine: a critical nutrient for future fish feeds. Aquaculture 437:215–229

    Article  CAS  Google Scholar 

  • Schaffert CS (2011) Role of MGST1 in reactive intermediate-induced injury. World J Gastroenterol 17:2552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sissener N, Waagbø R, Rosenlund G, Tvenning L, Susort S, Lea T, Oaland Ø, Chen L, Breck O (2016) Reduced n-3 long chain fatty acid levels in feed for Atlantic salmon (Salmo salar L.) do not reduce growth, robustness or product quality through an entire full scale commercial production cycle in seawater. Aquaculture 464:236–245

    Article  CAS  Google Scholar 

  • Torstensen BE, Bell JG, Rosenlund G, Henderson RJ, Graff IE, Tocher DR, Lie O, Sargent JR (2005) Tailoring of Atlantic salmon (Salmo salar L.) flesh lipid composition and sensory quality by replacing fish oil with a vegetable oil blend. J Agric Food Chem 53:10166–10178

    Article  CAS  PubMed  Google Scholar 

  • Torstensen BE, Espe M, Sanden M, Stubhaug I, Waagbø R, Hemre G-I, Fontanillas R, Nordgarden U, Hevrøy EM, Olsvik P, Berntssen MHG (2008) Novel production of Atlantic salmon (Salmo salar) protein based on combined replacement of fish meal and fish oil with plant meal and vegetable oil blends. Aquaculture 285:193–200

    Article  CAS  Google Scholar 

  • Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98:5116–5121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034

    Article  PubMed  PubMed Central  Google Scholar 

  • Vilhelmsson OT, Martin SAM, Médale F, Kaushik SJ, Houlihan DF (2004) Dietary plant-protein substitution affects hepatic metabolism in rainbow trout (Oncorhynchus mykiss). Br J Nutr 92:71–80

    Article  CAS  PubMed  Google Scholar 

  • Wamelink M, Struys E, Jakobs C (2008) The biochemistry, metabolism and inherited defects of the pentose phosphate pathway: a review. J Inherit Metab Dis 31:703–717

    Article  CAS  PubMed  Google Scholar 

  • Wilson R (1994) Utilization of dietary carbohydrate by fish. Aquaculture 124:67–80

    Article  CAS  Google Scholar 

  • Xu Q, Feng CY, Hori TS, Plouffe DA, Buchanan JT, Rise ML (2013) Family-specific differences in growth rate and hepatic gene expression in juvenile triploid growth hormone (GH) transgenic Atlantic salmon (Salmo salar). Comp Biochem Physiol Part D Genomics Proteomics 8:317–333

    Article  CAS  PubMed  Google Scholar 

  • Xue X, Hixson SM, Hori TS, Booman M, Parrish CC, Anderson DM, Rise ML (2015) Atlantic salmon (Salmo salar) liver transcriptome response to diets containing Camelina sativa products. Comp Biochem Physiol Part D Genomics Proteomics 14:1–15

  • Ye J, Kaattari IM, Ma C, Kaattari S (2013) The teleost humoral immune response. Fish Shellfish Immunol 35:1719–1728

    Article  CAS  PubMed  Google Scholar 

  • Zuo R, Ai Q, Mai K, Xu W, Wang J, Xu H, Liufu Z, Zhang Y (2012) Effects of dietary n-3 highly unsaturated fatty acids on growth, nonspecific immunity, expression of some immune related genes and disease resistance of large yellow croaker (Larmichthys crocea) following natural infestation of parasites (Cryptocaryon irritans). Fish Shellfish Immunol 32:249–258

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank Danny Boyce and the Dr. Joe Brown Aquatic Research Building staff (JBARB, Memorial University of Newfoundland, Canada) for their assistance with fish husbandry and sampling. We are grateful to Jeanette Wells for providing the tissue lipid composition, to Cara Kirkpatrick (Genome Atlantic, Canada) for her help as Program Manager for this project, to Dr. Dominic Nanton (Cargill Innovation, Norway) for feed formulations, to the lab team for assistance with sampling, to Dr. Surendra Kumar (Ocean Frontier Institute, Memorial University of Newfoundland, Canada) for providing new annotation of the 44K salmon microarray, and to ACENET (https://www.ace-net.ca/) and Compute Canada (https://www.computecanada.ca/) for providing computational resources utilized in updating the annotation of this 44K microarray.

Funding

This study was conducted within the Biomarker Platform for Commercial Aquaculture Feed Development project, a Genomic Applications Partnership Program (GAPP #6604), funded by the Government of Canada through Genome Canada and Genome Atlantic, and Cargill Innovation (formerly EWOS Innovation). MLR’s research program is also supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant (341304–2012). XX is supported by a Postgraduate Scholarship-Doctoral (PGS D) from NSERC and a Memorial University of Newfoundland SGS fellowship.

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  1. Department of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, A1C 5S7, Canada

    Xi Xue, Albert Caballero-Solares, Khalil Eslamloo, Christopher C. Parrish & Matthew L. Rise

  2. Aquatic Research Cluster, CREAIT Network, Ocean Sciences Centre, Memorial University of Newfoundland, St. John’s, NL, A1C 5S7, Canada

    Jennifer R. Hall

  3. Cargill Animal Nutrition, 10383 165th Avenue NW, Elk River, MN, 55330, USA

    Richard G. Taylor

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Correspondence to Albert Caballero-Solares.

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Author RGT, in the representation of Cargill Innovation, participated in the formulation of the experimental diets and the design of the trial, but had no role in the design of the gene expression experiment, the data collection and analysis, the preparation of this manuscript, and the decision to submit the manuscript for publication. All authors declare that they have no competing interests.

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Xue, X., Hall, J.R., Caballero-Solares, A. et al. Liver Transcriptome Profiling Reveals That Dietary DHA and EPA Levels Influence Suites of Genes Involved in Metabolism, Redox Homeostasis, and Immune Function in Atlantic Salmon (Salmo salar). Mar Biotechnol 22, 263–284 (2020). https://doi.org/10.1007/s10126-020-09950-x

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