Transcriptional development of phospholipid and lipoprotein metabolism in different intestinal regions of Atlantic salmon (Salmo salar) fry

Abstract

BackgroundIt has been suggested that the high phospholipid (PL) requirement in Atlantic salmon (Salmo salar) fry is due to insufficient intestinal de-novo synthesis causing low lipoprotein (LP) production and reduced transport capacity of dietary lipids. However, there has not been performed any in-depth ontological analysis of intestinal PL and LP synthesis with development of salmon. Therefore in this paper we used RNA-seq technology to test the hypothesis that the high PL requirement in salmon fry was associated with undeveloped PL synthesis and LP formation pathways in intestine. There was a special focus on the understanding homologous genes, especially from salmonid-specific fourth vertebrate whole-genome duplication (Ss4R), contribution to salmonid specific features of regulation of PL metabolic pathways. The study was performed in stomach, pyloric caeca and hindgut at 0.16g (1 day before first-feeding), 2.5g and 10g of salmon.ResultsIn general, we found an up-regulation of de-novo phosphatidylcholine (PtdCho) synthesis, phosphatidylethanolamine (PtdEtn) and LP formation pathways in pyloric caeca of salmon between 0.16g and 10g. Thirteen genes in these pathways were highly (q<0.05) up-regulated in 2.5g salmon compared to 0.16g, while only five more significant (q<0.05) genes were found when the fish grew up to 10g. Different homologous genes were found dominating in stomach, pyloric caeca and hindgut. However, the expression of dominating genes in PL and LP synthesis pathways was much higher in pyloric caeca than stomach and hindgut. Salmon-specific homologous (Ss4R) genes had similar expression during development, while other homologs had more diverged expression.ConclusionsAn increasing capacity for PL synthesis and LP formation was confirmed in pyloric caeca. The up-regulation of the de-novo PtdCho pathway confirms that the salmon fry have increasing requirement for dietary PtdCho compared to adult. The similar expressions between Ss4R homologous genes suggest that the functional divergence of these genes was incomplete compared to homologs derived from other whole genome duplication. The results of the present study have provided new information on the molecular mechanisms of phospholipid synthesis and lipoprotein formation in fish.

Diet and Life Stage-Associated Lipidome Remodeling in Atlantic Salmon

“…Dietary PLs in fish are predominately digested by phospholipase A2 into 1-acyl- sn -phospholipid (lyso-PL) and FFA, which are then absorbed and re-synthesized into new PLs in enterocytes by lysophospholipid acyltransferase (LPAT). 3 , 36 Our study has found higher amounts of PC-44:12 (DHA-DHA-PC) and PE-44:12 (DHA-DHA-PE) in salmon fed a FO diet, while fish fed a VO diet had higher amounts of PC-40:9 (likely 18:3 n -3-DHA-PC) and PC-38:8 (likely 16:0-DHA-PC). The high PL-DHA in both VO- and FO-fed salmon suggests that LPAT preferentially esterifies LC-HUFA over other fatty acids.…”

“…In parallel to the increased rate of lipid remodeling in the gut of SW salmon, we observed higher steady-state expression levels of genes involved in lipid transport pathways ( Figure 4 A). These genes include agpat 4 -a and chka-b , involved in de novo synthesis of glycerophospholipid, 36 , 37 genes mtp-a , sar 1 a-b , apobb , apoa 4 a-a , and apoa 1 -a involved in lipoprotein formation, 36 and gene fabp 2 a-b involved in intracellular transport of fatty acids. 38 In the liver, no difference was observed in the expression of genes involved in phospholipid and lipoprotein formation between the livers of SW salmon and FW salmon.…”

A systemic study of lipid metabolism regulation in salmon fingerlings and early juveniles fed plant oil

“…The raw sequences are publicly available on European Nucleotide Archive under accession number PRJEB21981. The raw sequence data for FO samples were used in a previous study to understand the transcriptional development of phospholipid and lipoprotein metabolism in salmon fry ( 8 ) .…”

“…Most studies on dietary lipid utilisation have focused on the pyloric caeca or midgut as they are the predominant regions for lipid absorption and transport in salmon ( 3 – 6 ) . The hindgut could also be involved in absorption and transport of lipids, as both histological and genetical studies have suggested an existence of lipoproteins in the region ( 7 , 8 ) . The stomach is primarily responsible for mechanical and chemical digestion of feed, but may also be involved in absorption of SCFA, Na and water ( 9 ) .…”

“…To date, approximately 55 % of the Ss4R gene duplicates are still retained as expressed genes in Atlantic salmon ( 32 ) . Some of the Ss4R duplicates have been found to have distinct regulation in different tissues ( 8 ) , developmental stages ( 8 ) and dietary treatment ( 22 ) . This has markedly increased the complexity of understanding lipid metabolism pathways in salmon, meaning the functional divergence of gene duplicates must be taken into consideration in diet-induced gene expression studies.…”