Abstract
Sirtuins (SIRTs) represent a conserved protein family of deacetylases that act as master regulators of metabolism, but little is known about their roles in fish and livestock animals in general. The present study aimed to assess the value of SIRTs for the metabolic phenotyping of fish by assessing their co-expression with a wide-representation of markers of energy and lipid metabolism and intestinal function and health in two genetically different gilthead sea bream strains with differences in growth performance. Fish from the fast-growing strain exhibited higher feed intake, feed efficiency and plasma IGF-I levels, along with higher hepatosomatic index and lower mesenteric fat (lean phenotype). These observations suggest differences in tissue energy partitioning with an increased flux of fatty acids from adipose tissue toward the liver. The resulting increased risk of hepatic steatosis may be counteracted in the liver by reduced lipogenesis and enhanced triglyceride catabolism, in combination with a higher and more efficient oxidative metabolism in white skeletal muscle. These effects were supported by co-regulated changes in the expression profile of SIRTs (liver, sirt1; skeletal muscle, sirt2; adipose tissue, sirt5-6) and markers of oxidative metabolism (pgc1α, cpt1a, cs, nd2, cox1), mitochondrial respiration uncoupling (ucp3) and fatty acid and triglyceride metabolism (pparα, pparγ, elovl5, scd1a, lpl, atgl) that were specific to each strain and tissue. The anterior intestine of the fast-growing strain was better suited to cope with improved growth by increased expression of markers of nutrient absorption (fabp2), epithelial barrier integrity (cdh1, cdh17) and immunity (il1β, cd8b, lgals1, lgals8, sIgT, mIgT), which were correlated with low expression levels of sirt4 and markers of fatty acid oxidation (cpt1a). In the posterior intestine, the fast-growing strain showed a consistent up-regulation of sirt2, sirt3, sirt5 and sirt7 concurrently with increased expression levels of markers of cell proliferation (pcna), oxidative metabolism (nd2) and immunity (sIgT, mIgT). Together, these findings indicate that SIRTs may play different roles in the regulation of metabolism, inflammatory tone and growth in farmed fish, arising as powerful biomarkers for a reliable metabolic phenotyping of fish at the tissue-specific level.
Highlights
The capacity of aquaculture to meet the future demand for seafood will largely depend on the use of highly efficient domesticated animal stocks
The resulting viscerosomatic (VSI) and mesenteric fat (MFI) indexes were significantly lower in fish of strain 1, whereas the opposite was observed for the hepatosomatic index (HSI)
The integration of transcriptomic profiles from two genetically different gilthead sea bream strains with differences in growth performance contributes to linking the molecular signature of sirtuin deacetylases/deacylases/ADP-ribosyltransferases (SIRTs) to downstream markers of energy and lipid metabolism and immunological/inflammatory status, which allows for improvement in intestinal health and more efficient nutrient utilization
Summary
The capacity of aquaculture to meet the future demand for seafood will largely depend on the use of highly efficient domesticated animal stocks. Less than 10% of the aquaculture production comes from genetically improved animals (Olesen et al, 2015); different selective breeding programs are in progress for most farmed European fish species, including the gilthead sea bream (Sparus aurata L.), a highly cultured perciform fish in all the Mediterranean basin. The application of genomic tools in aquaculture is in its infancy (McAndrew and Napier, 2011), and few gilthead sea bream companies are currently using marker-assisted selection (MAS) (Janssen et al, 2015). The identification of new candidate genes for MAS, for productive traits that are not easy to measure (e.g., feed efficiency, redox homeostasis, intestinal health), can be fueled using wide or targeted transcriptomic approaches (Chen et al, 2011; Cardoso et al, 2014; Choi et al, 2015). The interplay between nutrition and immune system is well recognized; the true integration of research on fish nutrition, growth, chronobiology, energy status, immune function and intestinal health is still far from clear despite recent and important advances in this field (Calduch-Giner et al, 2016; Estensoro et al, 2016; Martin and Król, 2017; Piazzon et al, 2017; Yúfera et al, 2017)
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