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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)

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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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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Correspondence to Albert Caballero-Solares.

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Conflict of Interest

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 (2020). https://doi.org/10.1007/s10126-020-09950-x

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Keywords

  • Hepatic transcriptome
  • DHA
  • EPA
  • Metabolism
  • Immune
  • Molecular biomarkers