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Muscular lipidomics and transcriptomics reveal the effects of bile acids on lipid metabolism in high-fat diet-fed grouper

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Abstract

Little information is available on how exogenous bile acids alter lipid metabolism in muscle of fish. In the present study, an 8-week feeding trial were used to investigate the impacts of bile acids on lipid deposition, lipid metabolism, lipidomics, and transcriptomics in muscle of pearl gentian grouper (Epinephelus fuscoguttatus♀ × E. lanceolatus♂) fed a high-fat diet (HD). The HD treatment significantly increased the crude lipid content, while bile acids diet (BD) treatment decreased it (p = 0.057). BD treatment significantly decreased triglycerides level and significantly increased phosphatidylcholines, phosphatidylethanolamines, and phosphatidylglycerol levels. The contents of TG (17:0/18:2/18:2), TG (17:1/18:2/22:6), PC (6:0/22:1), PC (9:0/26:1), PC (26:1/6:0), PC (17:2/18:2), PE (16:0/18:1), PE (18:0/17:1), PG (18:0/20:5), PG (18:3/20:5), PG (19:0/16:1), and PG (18:0/18:1) in muscle were well response to dietary lipid level and bile acids supplementation. HD and BD groups induced a variety of adaptive metabolic responses in transcriptomics. HD treatment increased the lipogenesis and decreased lipolysis, whereas BD treatment decreased the lipogenesis and increased lipolysis. Present study revealed the improvement of muscular lipid metabolism and lipid composition in response to bile acids administration in pearl gentian grouper.

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Data availability

The original data of lipidomics (accession ID: MTBLS4808) were deposited in MetaboLights database. The original transcriptomics reads were deposited in NCBI database (accession ID: PRJNA833953).

Abbreviations

4ebp :

Eukaryotic initiation factor 4E binding protein

aco :

Acyl-CoA oxidase 1

atgl :

Adipose triglyceride lipase

BD:

HD with 0.09% bile acids

CD:

Control diet

CE:

Cholesterol ester

Cer:

Ceramides

eif4b :

Eukaryotic initiation factor 4B

HD:

High-fat diet

LPC:

Lysophosphatidylcholine

LPE:

Lysophosphatidylethanolamine

LPG:

Lysophosphatidylglycerol

mtor :

Mammalian target of rapamycin

mlst8 :

Target of rapamycin complex subunit LST8

PC(O):

Alkylphosphatidylcholine

PC(P):

Alkenylphosphatidylcholine

PE:

Phosphatidylethanolamines

PE(P):

Alkenylphosphatidylethanolamine

PG:

Phosphatidylglycerol

PhytoCer:

Phytoceramides

PI:

Phosphatidylinositol

ppara :

Peroxisome proliferator-activated receptor alpha

ragab :

Ragulator-Rag complex A/B

ragcd :

Ragulator-Rag complex C/D

raptor :

Regulatory-associated protein of mTOR

s6 :

Ribosomal protein S6

s6k :

Ribosomal protein S6 kinase

srebp1 :

Sterol-regulator element-binding protein 1

tel2 :

Telomere length regulation protein

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Acknowledgments

We would like to acknowledge Suzhou BioNovoGene for providing technical help.

Funding

This work was supported by the National Key R&D Program of China (2019YFD0900200), the China Agriculture Research System of MOF and MARA (CARS-47), the Science and technology project of Zhanjiang (2020A05003), the Natural Science Foundation of Guangdong Province (2018A030313154&2020A1515011129), and the National Natural Science Foundation of China (no. 31772864).

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Authors and Affiliations

  1. Laboratory of Aquatic Animal Nutrition and Feed, Fisheries College, Guangdong Ocean University, Zhanjiang, 524088, China

    Jia Xu, Menglin Shi, Liutong Chen, Shuyan Chi, Shuang Zhang, Junming Cao, Beiping Tan & Shiwei Xie

  2. Guangxi Key Laboratory of Marine Environmental Science, Guangxi Academy of Marine Sciences, Guangxi Academy of Sciences, Nanning, China

    Jia Xu

  3. Key Laboratory of Aquatic, Livestock and Poultry Feed Science and Technology in South China, Ministry of Agriculture, Zhanjiang, China

    Shuyan Chi, Shuang Zhang, Junming Cao, Beiping Tan & Shiwei Xie

  4. Aquatic Animals Precision Nutrition and High Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang, China

    Shuyan Chi, Shuang Zhang, Junming Cao, Beiping Tan & Shiwei Xie

Authors
  1. Jia Xu
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  2. Menglin Shi
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  3. Liutong Chen
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  4. Shuyan Chi
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  7. Beiping Tan
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  8. Shiwei Xie
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Contributions

Conceptualization: Jia Xu, Menglin Shi, and Liutong Chen; methodology: Jia Xu, Menglin Shi, Liutong Chen, and Shiwei Xie; formal analysis and investigation: Jia Xu, Shuyan Chi, and Shuang Zhang; writing—original draft preparation: Jia Xu, Shuyan Chi, and Junming Cao; writing—review and editing: Jia Xu, Shuang Zhang, Junming Cao, and Shiwei Xie; funding acquisition: Beiping Tan and Shiwei Xie; resources: Junming Cao, Beiping Tan, and Shiwei Xie; supervision: Junming Cao, Beiping Tan, and Shiwei Xie. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Beiping Tan or Shiwei Xie.

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The experimental procedures were approved by the Animal Ethical and Welfare Committee of Guangdong Ocean University (Guangdong, China), processing ID: GDOU-AEWC-20180063.

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The authors declare no competing interests.

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Supplementary information

ESM 1:

Fig. S1 Quality control and lipid composition of lipidomics in groups. A: In PCA plot, the quality control sample is red and the tested sample is green. A smaller difference in quality control sample means a more stable system. B: the composition and numbers of lipid classes (n = 6). PC: phosphatidylcholines, PE: phosphatidylethanolamines, TG: triglycerides, DG: diacylglycerols, SM: sphingomyelins, CE: cholesterol ester, Cer: ceramides, LPC: lysophosphatidylcholine, LPE: lysophosphatidylethanolamine, LPG: lysophosphatidylglycerol, PC(O): alkylphosphatidylcholine, PC(P): alkenylphosphatidylcholine, PE: phosphatidylethanolamines, PE(P): alkenylphosphatidylethanolamine, PG: phosphatidylglycerol, PhytoCer: phytoceramides, PI: phosphatidylinositol. Fig. S2 PCA analysis of composition of SCM in TG (A), PC (B), PE (C) and PG (D) classes of muscle in CD, HD and BD groups (n = 6). TG: triglycerides, PC: phosphatidylcholines, PE: phosphatidylethanolamines, PG: phosphatidylglycerol. SCM: significantly changed metabolites. CD: control diet; HD: high-fat diet; BD: HD with 0.09% bile acids. Fig. S3 Heatmap analysis of composition of significantly changed metabolites in TG classes of muscle in CD, HD and BD groups (n = 6). TG: triglycerides. CD: control diet; HD: high-fat diet; BD: HD with 0.09% bile acids. Fig. S4 Heatmap analysis of composition of significantly changed metabolites in PC classes of muscle in CD, HD and BD groups (n = 6). PC: phosphatidylcholines. CD: control diet; HD: high-fat diet; BD: HD with 0.09% bile acids. Fig. S5 Heatmap analysis of composition of significantly changed metabolites in PE classes of muscle in CD, HD and BD groups (n = 6). PE: phosphatidylethanolamines. CD: control diet; HD: high-fat diet; BD: HD with 0.09% bile acids. Fig. S6 Heatmap analysis of composition of significantly changed metabolites in PG classes of muscle in CD, HD and BD groups (n = 6). PG: phosphatidylglycerol. CD: control diet; HD: high-fat diet; BD: HD with 0.09% bile acids. Fig. S7 KEGG enrichment pathways (top 20) of global DEGs profile of muscle in CD, HD and BD groups (n = 3). A: According to the p value, the results of DEGs profile in CD and HD groups. B: According to the p value, the results of DEGs profile in HD and BD groups. C: According to the FDR, the results of DEGs profile in CD and HD groups. D: According to the FDR, the results of DEGs profile in HD and BD groups. In C and D panels, the X-axis represents the Rich Factor, and Y-axis represents the name of a metabolic pathway. The Rich Factor is the ratio of a to b. a: the amount of DEGs in one pathway; b: the amount of all genes in this pathway. DEGs: differentially expressed genes; CD: control diet; HD: high-fat diet; BD: HD with 0.09% bile acids. Fig. S8 The WB original image of PPARA. Fig. S9 The WB original image of GAPDH. Fig. S10 The WB original image of SREBP1. Fig. S11 The WB original image of P-PPARA. (DOCX 3133 kb)

ESM 2:

Table S1 Composition and concentration of nutrients in diets (XLSX 10 kb)

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Table S2 Composition of fatty acids in diets (XLSX 12 kb)

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Table S3 Primers designed for qPCR (XLSX 10 kb)

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Table S4 The identified lipid species and composition in muscle of pearl gentian grouper in three groups (XLSX 465 kb)

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Table S5 The composition of lipid calsses in three groups (XLSX 10 kb)

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Table S6 Significantly changed metabolites in TG classes (XLSX 30 kb)

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Table S7 Significantly changed metabolites in PC classes (XLSX 59 kb)

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Table S8 Significantly changed metabolites in PE classes (XLSX 26 kb)

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Table S9 Significantly changed metabolites in PG classes (XLSX 17 kb)

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Table S10 Summary statistics of the muscle transcriptomics assembly of pearl gentian grouper (XLSX 9 kb)

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Table S11 Differentially expressed genes in all groups (XLSX 2351 kb)

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Table S12 KEGG enrichment pathways in three groups (XLSX 9 kb)

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Table S13 The differentially expressed genes related to lipid metabolism and amino acid metabolism in three groups (XLSX 10 kb)

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Xu, J., Shi, M., Chen, L. et al. Muscular lipidomics and transcriptomics reveal the effects of bile acids on lipid metabolism in high-fat diet-fed grouper. Fish Physiol Biochem 50, 127–143 (2024). https://doi.org/10.1007/s10695-023-01176-7

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