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, in-depth ontogenetic analysis of intestinal PL and LP synthesis with the development of salmon has yet to be performed. Therefore, in this paper we used RNA-Seq technology to investigate the expression of genes involved in PL synthesis and LP formation throughout early developmental stages and associate insufficient expression of synthesis pathways in salmon fry with its higher dietary PL requirement. There was a special focus on the understanding homologous genes, especially those from salmonid-specific fourth vertebrate whole-genome duplication (Ss4R), and their contribution to salmonid specific features of regulation of PL metabolic pathways. Salmon fry were sampled at 0.16 g (1 day before first-feeding), 2.5 and 10 g stages of development and transcriptomic analysis was applied separately on stomach, pyloric caeca and hindgut of the fish.ResultsIn general, we found up-regulated pathways involved in synthesis of phosphatidylcholine (PtdCho), phosphatidylethanolamine (PtdEtn), and LP in pyloric caeca of salmon between 0.16 and 10 g. Thirteen differentially expressed genes (q < 0.05) in these pathways were highly up-regulated in 2.5 g salmon compared to 0.16 g, while only five more differentially expressed (q < 0.05) genes were found when the fish grew up to 10 g. Different homologous genes were found dominating in stomach, pyloric caeca and hindgut. However, the expression of dominating genes in pathways of PL and LP synthesis were much higher in pyloric caeca than stomach and hindgut. Salmon-specific homologous genes (Ss4R) had similar expression during development, while other homologs had more diverged expression.ConclusionsThe up-regulation of the de-novo PtdCho and PtdEtn pathways confirm that salmon have decreasing requirement for dietary PL as the fish develops. The similar expressions between Ss4R homologous genes suggest that the functional divergence of these genes was incomplete compared to homologs derived from other genome duplication. The results of the present study have provided new information on the molecular mechanisms of phospholipid synthesis and lipoprotein formation in fish.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4651-8) contains supplementary material, which is available to authorized users.

Comparative transcriptomics reveals domestication‐associated features of Atlantic salmon lipid metabolism

“…The method for handling RNA‐seq data has been described in detail in previous studies (Gillard et al., 2018; Jin et al., 2018). In brief, read sequences were quality trimmed using cutadapt (version 1.8.1) before being aligned to the salmon genome ( icsasg _version 2).…”

“…To visualize expression levels between different genes and tissues, normalized counts in the form of transcripts per million (TPM) values were generated. Raw gene counts were first divided by their mRNA length in kilobases to normalize for transcript length, and then divided by the total number of counts from each library to normalize for sequencing depth (Jin et al., 2018).…”

Comparative transcriptomics reveals domestication-associated features of Atlantic salmon lipid metabolism

“…We approach this question by 93 running a feeding trial with both domesticated and wild salmon that are fed contrasting diets 94 rich in either FO, VO or PL and then perform comparative transcriptomic and fatty acid 95 analyses of two tissues involved in lipid uptake (pyloric caeca) and endogenous synthesis of 96 LC-PUFAs (liver). Our study shows clear differences between metabolism in the wild and 97 domestic salmon genetic backgrounds and suggests that the regulation of genes involved in 98 The method for handling RNA-sequencing (RNA-seq) data has been described in detail in 165 previous studies (Gillard et al, 2018;Jin et al, 2018). In brief, read sequences were quality 166 trimmed using Cutadapt (v1.8.1) before being aligned to the salmon genome (ICSASG_v2).…”

“…In line with this idea, our study found that apoa1_2 gene was strikingly higher 441 expressed in liver in domesticated compared to wild salmon, regardless of dietary lipid 442 composition ( Figure 5). Although the existence of lipoproteins and their apolipoprotein 443 composition is not well described in fish, it is suggested that they should be similar to mammals 444 (Jin et al, 2018). The higher expression levels of apoa1_2 transcripts could therefore be one 445 factor that contributes to fast growth of domesticated salmon, as this gene is key to the 446 lipoprotein assembly and thereby transport of lipids between liver and other tissues such as 447 muscle and adipose tissue (Xu et al, 2013).…”

“…For visualize expression levels between different genes and 209 tissues, normalized counts in the form of transcripts per million (TPM) values were generated. 210Raw gene counts were first divided by their mRNA length in kilobases to normalize for 211 transcript length, and then divided by the total number of counts from each library to 212 normalize for sequencing depth(Jin et al, 2018). 213 214 Statistical analysis of fish weight and fatty acids composition was also performed in R. 215 Two-way ANOVA with Tukey HSD post hoc test was used to test the effect of strain and diet 216 on fish weight and fatty acids composition of each lipid class, tissue and sampling day.…”