Abstract
Yellow head catfish, Pelteobagrus fulvidraco, with delicious meat and high commercial value has relatively high lipid accumulation which is considered to be a major problem in aquaculture. It was found that fucoidan has the functions in reducing lipid concentration and enhancing the immunity capability. The purpose of this study is to understand the role of fucoidan in juvenile yellow head catfish and the underlying comprehensive lipid metabolic regulation. The overall changes of significant lipid biomarkers in juvenile yellow head catfish fed on 0.1% fucoidan at different time points were studied by ultra-performance liquid chromatography coupled with quadrupole time-of-flight mass spectrometry (UPLC-ESI-Q-TOF-MS) and multivariate statistical analysis. At the eighth week, the lipid profile had the largest difference between the two groups, with 10 lipids identified as potential lipid biomarkers. Lysophosphatidylcholine (Lyso-PC), phosphatidylcholine (PC), and phosphatidylethanolamine (PE) were elevated, while triglycerides (TAGs) were reduced in SF group compared to C group. Overall, the content of free fatty acids (FFAs), derived from TAG, was decreased, whereas that of total fatty acids (TFAs) derived from FFAs showed the opposite tendency. Fucoidan can reduce the content of triglyceride perhaps by altering the activities of related enzymes and improve immunity capability of the juvenile yellow head catfish through increasing the whole levels of related fatty acids, which may be useful for facilitating efficient development and scientific improvement of fishery.
Similar content being viewed by others
Abbreviations
- UPLC:
-
Ultra-performance liquid chromatography
- Q-TOF-MS:
-
Quadrupole time-of-flight mass spectrometry
- MS/MS:
-
Tandem mass spectrometry
- TIC:
-
Total ion current chromatogram
- EIC:
-
Extracted ion chromatogram
- ESI:
-
Electrospray ionization
- RT:
-
Retention time
- GC-MS:
-
Gas chromatography coupled with mass spectrometry
- BHT:
-
Butylated hydroxytoluene
- PCA:
-
Principal component analysis
- PLS-DA:
-
Projections to latent structure discriminant analysis
- OPLS-DA:
-
Orthogonal projections to latent structure discriminant analysis
- PC:
-
Phosphatidylcholine
- Lyso-PC:
-
Lysophosphatidylcholine
- PE:
-
Phosphatidylethanolamine
- PI:
-
Phosphatidylinositol
- DAG:
-
Diacylglycerol
- TAG:
-
Triacylglycerol
- Cer:
-
Ceramide
- GP:
-
Glycerophospholipid
- SM:
-
Sphingomyelin
- TFAs:
-
Total fatty acids
- FFAs:
-
Free fatty acids
- PUFAs:
-
Polyunsaturated fatty acids
- SFAs:
-
Saturated fatty acids
- MUFAs:
-
Monounsaturated fatty acids
- TC:
-
Total cholesterol
- HDL-C:
-
High-density lipoprotein cholesterol
- GLU:
-
Glucose
- LPL:
-
Lipoprotein lipase
- MAGs:
-
Monoacylglycerols
- FBW:
-
Final body weight
- WGR:
-
Weight gain rate
- SGR:
-
Specific growth rate
- FCR:
-
Feed conversion ratio
- PER:
-
Protein efficiency rate
- SD:
-
Standard deviation
- QC:
-
Quality control
- SF:
-
Sargassum fucoidan
- LCB:
-
Long-chain base
References
Berteau O, Mulloy B (2003) Sulfated fucans, fresh perspectives: structures, functions, and biological properties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide. Glycobiology 13:29R–40R
Bylesjö M, Rantalainen M, Cloarec O, Nicholson JK, Holmes E, Trygg J (2006) OPLS discriminant analysis: combining the strengths of PLS-DA and SIMCA classification. J Chemom 20:341–351
Casas-Agustench P, Sloan S, Jacques P, Willinger C, Yin X, Courchesne P (2014) Connections between dark fish intake, lipidomics and plasma triglycerides in the Framingham heart study. Atherosclerosis 235:e186
Chen DY, Yan XJ, Xu JL, Su XL, Li LJ (2013a) Lipidomic profiling and discovery of lipid biomarkers in Stephanodiscus sp. under cold stress. Metabolomics 9:949–959
Chen QL, Gong Y, Luo Z, Zheng JL, Zhu QL (2013b) Differential effect of waterborne cadmium exposure on lipid metabolism in liver and muscle of yellow catfish Pelteobagrus fulvidraco. Aquatic Toxicol 142:380–386
Chen QL, Luo Z, Tan XY, Pan YX, Zheng JL, Zou M (2014) Molecular cloning and mRNA tissue expression of thyroid hormone receptors in yellow catfish Pelteobagrus fulvidraco and javelin goby Synechogobius hasta. Gene 536:232–237
Chen JJ, Li M, Yang R, Luo QJ, Xu JL, Ye YF, Yan XJ (2016) Profiling lipidome changes of Pyropia haitanensis in short-term response to high-temperature stress. J App Phycol: 1–11
Ganesan S, Shabits BN, Zaremberg V (2015) Tracking diacylglycerol and phosphatidic acid pools in budding yeast. Lipid Insights 8(Suppl 1):75
Gao YH, Lu YH, Huang SM, Gao L, Liang XX, Wu YN (2014) Identifying early urinary metabolic changes with long-term environmental exposure to cadmium by mass-spectrometry-based metabolomics. Environ Sci Technol 48:6409–6418
Han X (2009) Lipidomics: developments and applications. J Chromatogr B Anal Technol Biomed Life Sci 877:2663
Han X, Gross RW (2003) Global analyses of cellular lipidomes directly from crude extracts of biological samples by ESI mass spectrometry a bridge to lipidomics. J Lipid Res 44:1071–1079
Hermansson M, Uphoff A, Käkelä R, Somerharju P (2005) Automated quantitative analysis of complex lipidomes by liquid chromatography/mass spectrometry. Anal Chem 77:2166–2175
Huang F, Yan AS, Xiong CX (1999) Evaluation of the nutrition and the rate or flesh in the whole body of Pelteobagraus fulvidraco rich. FRESHWATER FISHERIES 10:000
Huang J, Chen Q, Nong YH, Ke YE, Chen YM, Cai ZD (2000) Study on flesh content and its nutritive value of Pseudobagrus fulvidraco (Richardson). J Agric Bio Sci 20:45–50
Kim KJ, Lee OH, Lee BY (2010) Fucoidan, a sulfated polysaccharide, inhibits adipogenesis through the mitogen-activated protein kinase pathway in 3T3-L1 preadipocytes. Life Sci 86:791–797
Küpper FC, Gaquerel E, Boneberg EM, Morath S, Salaün JP, Potin P (2006) Early events in the perception of lipopolysaccharides in the brown alga Laminaria digitata include an oxidative burst and activation of fatty acid oxidation cascades. J Exp Bot 57:1991–1999
Leiro JM, Castro R, Arranz JA, Lamas J (2007) Immunomodulating activities of acidic sulphated polysaccharides obtained from the seaweed Ulva rigida C. Agardh. Int Immunopharmacol 7:879–888
Li B, Lu F, Wei XJ, Zhao RX (2008) Fucoidan: structure and bioactivity. Molecules 13:1671–1695
Li XF, Liu WB, Lu KL, Xu WN, Wang Y (2012) Dietary carbohydrate/lipid ratios affect stress, oxidative status and non-specific immune responses of fingerling blunt snout bream, Megalobrama amblycephala. Fish Shellfish Immunol 33:316–323
Li S, Xu JL, Chen J, Chen JJ, Zhou CX, Yan XJ (2014) Structural elucidation of co-eluted triglycerides in the marine diatom model organism Thalassiosira pseudonana by ultra-performance liquid chromatography/quadrupole time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 28:245–255
Linting M, van Os BJ, Meulman JJ (2011) Statistical significance of the contribution of variables to the PCA solution: an alternative permutation strategy. Psychometrika 76:440–460
Luo Z, Liu YJ, Mai KS, Tian LX, Liu DH, Tan XY, Lin HZ (2005) Effect of dietary lipid level on growth performance, feed utilization and body composition of grouper Epinephelus coioides juveniles fed isonitrogenous diets in floating netcages. Aquac Int 13:257–269
Luo Z, Tan XY, Zheng JL, Chen QL, Liu CX (2011) Quantitative dietary zinc requirement of juvenile yellow catfish Pelteobagrus fulvidraco, and effects on hepatic intermediary metabolism and antioxidant responses. Aquaculture 319:150–155
Park MK, Jung U, Roh C (2011) Fucoidan from marine brown algae inhibits lipid accumulation. Mar Drugs 9:1359–1367
Pisani LF, Lecchi C, Invernizzi G, Sartorelli P, Savoini G, Ceciliani F (2009) In vitro modulatory effect of ω-3 polyunsaturated fatty acid (EPA and DHA) on phagocytosis and ROS production of goat neutrophils. Vet Immunol Immunopathol 131:79–85
Ponce NM, Pujol CA, Damonte EB, Flores L, Stortz CA (2003) Fucoidans from the brown seaweed Adenocystis utricularis: extraction methods, antiviral activity and structural studies. Carbohydr Res 338:153–165
Puangkaew J, Kiron V, Somamoto T, Okamoto N, Satoh S, Takeuchi T (2004) Nonspecific immune response of rainbow trout (Oncorhynchus mykiss Walbaum) in relation to different status of vitamin E and highly unsaturated fatty acids. Fish Shellfish Immunol 16:25–39
Pulfer M, Murphy RC (2003) Electrospray mass spectrometry of phospholipids. Mass Spectrom Rev 22:332–364
Rainville PD, Stumpf CL, Shockcor JP, Plumb RS, Nicholson JK (2007) Novel application of reversed-phase UPLC-oaTOF-MS for lipid analysis in complex biological mixtures: a new tool for lipidomics. J Proteome Res 6:552–558
Reid BN, Ables GP, Otlivanchik OA, Schoiswohl G, Zechner R, Blaner WS (2008) Hepatic overexpression of hormone-sensitive lipase and adipose triglyceride lipase promotes fatty acid oxidation, stimulates direct release of free fatty acids, and ameliorates steatosis. J Biol Chem 283:13087–13099
Saera-Vila A, Calduch-Giner JA, Gómez-Requeni P, Médale F, Kaushik S, Pérez-Sánchez J (2005) Molecular characterization of gilthead sea bream (Sparus aurata) lipoprotein lipase. Transcriptional regulation by season and nutritional condition in skeletal muscle and fat storage tissues. Comp Biochem Phys B: Biochem Mol Biol 142:224–232
Sheridan MA (1988) Lipid dynamics in fish: aspects of absorption, transportation, deposition and mobilization. Comp Biochem Phys B: Comp Biochem 90:679–690
Spector AA (2001) Plasma free fatty acid and lipoproteins as sources of polyunsaturated fatty acid for the brain. J Mol Neurosci 16:159–165
Su XL, Xu JL, Yan XJ, Zhao P, Chen JJ, Zhou CX (2013) Lipidomic changes during different growth stages of Nitzschia closterium f. Minutissima. Metabolomics 9:300–310
Tan XY, Luo Z, Liu CX, Xie CX (2011) Dietary copper requirement of juvenile yellow catfish Pelteobagrus fulvidraco. Aquac Nutr 17:170–176
Tissot B, Montdargent B, Chevolot L, Varenne A, Descroix S, Gareil P, Daniel R (2003) Interaction of fucoidan with the proteins of the complement classical pathway. BBA-Proteins Proteom 1651:5–16
Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184
Toh DF, New LS, Koh HL, Chan ECY (2010) Ultra-high performance liquid chromatography/time-of-flight mass spectrometry (UHPLC/TOFMS) for time-dependent profiling of raw and steamed Panax notoginseng. J Pharmaceut Biomed 52:43–50
Waagbo R, Hemre GI, Holm J (1995) Tissue fatty acid composition, haematology and immunity in adult cod, Gadus morhua L., fed three dietary lipid sources. J Fish Dis 18:615–622
Wang XM (2004) Lipid signaling. Curr Opin Plant Biol 7:329–336
Wang XM, Devaiah SP, Zhang WH, Welti R (2006) Signaling functions of phosphatidic acid. Prog Lipid Res 45:250–278
Wang J, Zhang QB, Zhang ZS, Song HF, Li PC (2010) Potential antioxidant and anticoagulant capacity of low molecular weight fucoidan fractions extracted from Laminaria japonica. Int J Biol Macromol 46:6–12
Wang J, Zhang QB, Zhang ZS, Hou Y, Zhang H (2011) In-vitro anticoagulant activity of fucoidan derivatives from brown seaweed Laminaria japonica. Chin J Oceanol Limnol 29:679
Wenk MR (2005) The emerging field of lipidomics. Nat Rev Drug Discov 4:594–610
Wu QH, Rong XL, Xing YH, Li SW (2007) Regulatory mechanism of fucoidan for disorder of lipid metabolism in rats. Traditional Chin Drug Res Clin Pharmacol 18:434
Xu JL, Chen DY, Yan XJ, Chen JJ, Zhou CX (2010) Global characterization of the photosynthetic glycerolipids from a marine diatom Stephanodiscus sp. by ultra performance liquid chromatography coupled with electrospray ionization-quadrupole-time of flight mass spectrometry. Anal Chim Acta 663:60–68
Xu JL, Zhou HB, Yan XJ, Zhou CX, Zhu P, Ma B (2012) Effect of unialgal diets on the composition of fatty acids and sterols in juvenile ark shell Tegillarca granosa Linnaeus. J Agric Food Chem 60:3973–3980
Yan XJ, Li HY, Xu JL, Zhou CX (2010) Analysis of phospholipids in microalga Nitzschia closterium by UPLC-Q-TOF-MS. Chin J Oceanol Limnol 28:106–112
Yan XJ, Xu JL, Chen JJ, Chen DY, Xu SL, Luo QJ, Wang YJ (2012) Lipidomics focusing on serum polar lipids reveals species dependent stress resistance of fish under tropical storm. Metabolomics 8:299–309
Yang Q, Yang R, Li M, Zhou QC, Liang XP, Elmada ZC (2014) Effects of dietary fucoidan on the blood constituents, anti-oxidation and innate immunity of juvenile yellow catfish (Pelteobagrus fulvidraco). Fish Shellfish Immunol 41:264–270
Yokota T, Nagashima M, Ghazizadeh M, Kawanami O (2009) Increased effect of fucoidan on lipoprotein lipase secretion in adipocytes. Life Sci 84:523–529
Zehethofer N, Pinto DM (2008) Recent developments in tandem mass spectrometry for lipidomic analysis. Anal Chim Acta 627:62–70
Zhu S, Ye MW, Xu JL, Guo CY, Zheng HK, Hu JB (2015) Lipid profile in different parts of edible jellyfish Rhopilema esculentum. J Agric Food Chem 63:8283–8291
Acknowledgements
This work was financially supported by the Natural Science Foundation of Zhejiang Province of China (LY17D060005), Science Technology Department of Zhejiang Province (grant number 2016C37090), Natural Science Foundation of Ningbo of China (2015A 610266), China Spark Program (2015GA701027 and 2015GA701054), and K.C. Wong Magna Fund in Ningbo University. We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Xu, P., Wang, Y., Chen, J. et al. Lipidomic profiling of juvenile yellow head catfish (Pelteobagrus fulvidraco) in response to Fucoidan diet. Aquacult Int 25, 1123–1143 (2017). https://doi.org/10.1007/s10499-016-0102-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-016-0102-1