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

Jin, Yang; Olsen, Rolf Erik; Gillard, Gareth Benjamin; Östensen, Mari‐Ann; Korsvoll, Sven Arild; Santi, Nina; Vik, Jon Olav; Sandve, Simen Rød; Ôlsen, Yngvar

doi:10.1017/s0007114518001885

Cited by 17 publications

(14 citation statements)

References 59 publications

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“…The pyloric ceca of fish plays a key role in digestion and absorption, functioning in enzymatic digestion and nutrient absorption, including lipid digestion (Williams 2019 ; Buddington and Diamond 1987 ; Stevens and Hume 1995 ). Similar to our results, the pyloric ceca transcriptome of salmon fingerlings fed varying oil (Jin et al 2018 ) or carbohydrate (Betancor et al 2018 ) sources upregulated genes involved in lipid metabolism. In prickleback fishes, we found that wild fishes upregulate genes involved in protein, carbohydrate, and lipid metabolism and converting nutrients to energy storage in the pyloric ceca, yet we do not see this pattern in fishes fed the LO and LC diets.…”

Section: Discussionsupporting

confidence: 91%

Comparative transcriptomics reveal tissue level specialization towards diet in prickleback fishes

2022

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Beyond a few obvious examples (e.g., gut length, amylase activity), digestive and metabolic specializations towards diet remain elusive in fishes. Thus, we compared gut length, δ13C and δ15N signatures of the liver, and expressed genes in the intestine and liver of wild-caught individuals of four closely-related, sympatric prickleback species (family Stichaeidae) with different diets: Xiphister mucosus (herbivore), its sister taxon X. atropurpureus (omnivore), Phytichthys chirus (omnivore) and the carnivorous Anoplarchus purpurescens. We also measured the same parameters after feeding them carnivore or omnivore diets in the laboratory for 4 weeks. Growth and isotopic signatures showed assimilation of the laboratory diets, and gut length was significantly longer in X. mucosus in comparison to the other fishes, whether in the wild, or in the lab consuming the different diets. Dozens of genes relating to digestion and metabolism were observed to be under selection in the various species, but P. chirus stood out with some genes in the liver showing strong positive selection, and these genes correlating with differing isotopic incorporation of the laboratory carnivore diet in this species. Although the intestine showed variation in the expression of hundreds of genes in response to the laboratory diets, the liver exhibited species-specific gene expression patterns that changed very little (generally <40 genes changing expression, with P. chirus providing an exception). Overall, our results suggest that the intestine is plastic in function, but the liver may be where specialization manifests since this tissue shows species-specific gene expression patterns that match with natural diet.

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Section: Discussionsupporting

confidence: 91%

Comparative transcriptomics reveal tissue level specialization towards diet in prickleback fishes

2022

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“…Genes of cholesterol metabolism including hmgcrab, mvd-a and sqlea-a were only highly up-regualted in WT fed plant oil diet versus fish oil, while no transcription change was observed in Δ6abc/5 Mt versus WT salmon. Several studies have found up-regualtion of choleserol biosyntheis and srebp2 genes in salmon fed plant oils [11, 12, 14]. The present study has supported that the relationship between srebp2 and cholesterol biosynthesis genes is quite conserved as in salmon as in mammals, and suggests that the SREBP binding sites of cholesterol biosynthesis genes were srebp2 -specific [41].…”

Section: Resultssupporting

confidence: 82%

“…Additionally, sterol biosynthesis pathway was enriched for DEGs between WT salmon fed plant oil and fish oil but was not enriched for the DEGs between fads2 mutants versus WT fish (Figure 5 B). Indicating that the LC-HUFA level and PPAR has little effect on cholesterol biosynthesis in salmon, which should be more likely regulated by other biochemical signals such as low cholesterol level and other transcription factors including sterol regulatory binding protein 2 (SREBP2) [11, 12, 14]. More detailed discussion on PPAR and SREBP regulations will be shown later in this paper.…”

Section: Resultsmentioning

confidence: 99%

Targeted mutagenesis of Δ5 and Δ6 fatty acyl desaturases induce multiplex-mutagenesis and lipogenesis in Atlantic salmon (Salmo salar)

Jin

Datsomor

Olsen

et al. 2020

Preprint

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With declining wild fish populations, farmed Atlantic salmon (Salmo salar) has gained popularity as a source for healthy long-chain highly unsaturated fatty acids (LC-HUFA) including 20:5n-3 and 22:6n-3. However, the introduction of plant-based oil in fish diets has reduced the content of these beneficial LC-HUFA. The capability of biosynthesis of LC-HUFAs depends on fatty acids supplied in diets and the genetic potential residing in the fish. Key proteins involved in LC-HUFA synthesis in salmon include fatty acid desaturases 2 (Fads2). In a recent study we used CRISPR/Cas9 to generate two F0 mutant strains of salmon, 1) Δ6abc/5Mt with mutations in Δ5fads2, Δ6fads2-a, Δ6fads2-b and Δ6fads2-c genes, and 2) Δ6bcMt with mutations in Δ6fads2-b and Δ6fads2-c genes. The CRISPR mutated salmon (crispants) had reduced levels of LC-HUFA and expression of targeted fads2 genes. In present study we apply whole transcriptome analysis on these fads2 crispants. Our purpose is to evaluate the genetic mosaicism in fads2 crispants and the effect these mutations had on other lipid metabolism pathways in fish. Both Δ6abc/5Mt and Δ6bcMt crispants demonstrated high percentage of indels within all intended target genes, though different indel types and percentage were observed between individuals. Skipping of a CRISPR-targeted exon was observed in Δ6fads2-a gene of Δ6abc/5Mt salmon. The Δ6abc/5Mt fish also displayed several disruptive indels which resulted in over 100 differentially expressed genes (DEGs) enriched in lipid metabolism pathways in liver. This includes up-regulation of srebp1 genes as well as genes involved in fatty acid de-novo synthesis, fatty acid β-oxidation and lipogenesis. Both elovl5 and elovl2 genes were not changed, suggesting that the genes were not targeted by Srebp1. The mutation of Δ6bcMt surprisingly resulted in over 3000 DEGs which were enriched in factors encoding genes involved in mRNA regulation and stability.

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“…com/ articles/ suppl/ m011 p031_ supp. pdf, while data on host responses are published elsewhere (Jin et al 2018).…”

Section: Experimental Designmentioning

confidence: 99%

Atlantic salmon raised with diets low in long-chain polyunsaturated n-3 fatty acids in freshwater have a Mycoplasma-dominated gut microbiota at sea

Jin¹,

Angell²,

Sandve³

et al. 2019

Aquacult. Environ. Interact.

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Factors affecting the establishment of the gut microbiota in animals living in marine environments remain largely unknown. In terrestrial animals, however, it is well established that the juvenile environment has a major impact on the gut microbiota later in life. Atlantic salmon Salmo salar is an anadromous fish important in aquaculture with a juvenile freshwater stage and an adult seawater stage. For wild salmon, there are major dietary changes with respect to availability of long-chain polyunsaturated n-3 fatty acids (LC-n-3 PUFA) with lower abundance in freshwater systems. The aim of our work was therefore to determine the effect of a juvenile freshwater diet with high LC-n-3 PUFA, as compared to a diet low in LC-n-3 PUFA (designed to increase the endogenous LC-n-3 PUFA production), on the transition to a seawater gut microbiota for Atlantic salmon. We found a juvenile freshwater microbiota high in Firmicutes for fish raised with low LC-n-3 PUFA, while the microbiota for fish given high LC-n-3 PUFA feed was high in Proteobacteria. One hundred days after transfer to a common sea cage, fish that were given low LC-n-3 PUFA diets in freshwater showed significantly higher (p = 0.02, Kruskal-Wallis) Mycoplasma content (90 ± 7%; mean ± SD) compared to fish raised on a high LC-n-3 PUFA diet in freshwater (25 ± 31% Mycoplasma). Shotgun metagenome sequencing from fish raised with a low LC-n-3 PUFA diet identified a salmon-associated Mycoplasma in sea, being distinct from currently known Mycoplasma. The genome sequence information indicated a mutualistic lifestyle of this bacterium. Mycoplasma has also previously been identified as dominant (> 70%) in sea-living adult Atlantic salmon. Taken together, our results suggest that the juvenile freshwater diet influences the establishment of the gut microbiota in marine Atlantic salmon.

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

Cited by 17 publications

References 59 publications

Comparative transcriptomics reveal tissue level specialization towards diet in prickleback fishes

Comparative transcriptomics reveal tissue level specialization towards diet in prickleback fishes

Targeted mutagenesis of Δ5 and Δ6 fatty acyl desaturases induce multiplex-mutagenesis and lipogenesis in Atlantic salmon (Salmo salar)

Atlantic salmon raised with diets low in long-chain polyunsaturated n-3 fatty acids in freshwater have a Mycoplasma-dominated gut microbiota at sea

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