Skip to main content

Advertisement

Log in

Atlantic cod (Gadus morhua) larvae can biosynthesis phospholipid de novo from 2-oleoyl-glycerol and glycerol precursors

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

The dietary requirement of phospholipid (PL) of fish larvae has been suggested to originate in an inefficient ability for de novo biosynthesis of PL based on dietary triacylglycerol (TAG). The main objective of the present study was to investigate whether cod larvae could synthesis PL from sn-2-monoacylglycerol (2-MAG) and glycerol precursors. A tube feeding method was used to deliver equal molar aliquots of 2-oleoyl-[1,2,3-3H]glycerol and [U-14C] glycerol together with bovine serum albumin (BSA) bound 16:0 (palmitic acid) and 22:6n-3 (docosahexaenoic acid, DHA), with or without choline chloride to the foregut of anesthetized cod larvae and thereafter monitoring the metabolism of these components in the larvae through 4 h following injection. Our results showed that both 2-MAG and glycerol precursors contributed to the de novo synthesis of phosphatidylcholine (PC) and the 2-MAG pathway predominated over the G-3-P (glycerol-3-phosphate) pathway in the synthesis of TAG and PC. The molecular ratio of PC/TAG obtained from the 2-MAG and the G-3-P pathways was 0.44–0.74 and 1.02–2.06 within the first hour of tube feeding, suggesting they might have comparable biosynthesis ability of PC and TAG under the conditions of the present study. Furthermore, supplementation of choline chloride significantly increased PC/TAG ratio (p < 0.05) for both pathways. However, further studies are needed to quantify the enzyme activity involved in the CDP-choline (cytidine diphosphate choline) pathway, and the function of choline either in simulating PC synthesis or TAG catabolism or both needs further investigation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Attramadal KJK, Truong TMH, Bakke I, Skjermo J, Olsen Y, Vadstein O (2014) RAS and microbial maturation as tools for K-selection of microbial communities improve survival in cod larvae. Aquaculture 432:483–490. doi:10.1016/j.aquaculture.2014.05.052

    Article  Google Scholar 

  • Cahu CL, Gisbert E, Villeneuve LAN, Morais S, Hamza N, Wold PA, Infante JLZ (2009) Influence of dietary phospholipids on early ontogenesis of fish. Aquac Res 40:989–999. doi:10.1111/j.1365-2109.2009.02190.x

    Article  CAS  Google Scholar 

  • Dapra F, Geurden I, Corraze G, Bazin D, Zambonino-Infante JL, Fontagne-Dicharry S (2011) Physiological and molecular responses to dietary phospholipids vary between fry and early juvenile stages of rainbow trout (Oncorhynchus mykiss). Aquaculture 319:377–384. doi:10.1016/j.aquaculture.2011.07.016

    Article  CAS  Google Scholar 

  • DeLong CJ, Shen YJ, Thomas MJ, Cui Z (1999) Molecular distinction of phosphatidylcholine synthesis between the CDP-choline pathway and phosphatidylethanolamine methylation pathway. J Biol Chem 274:29683–29688. doi:10.1074/jbc.274.42.29683

    Article  CAS  PubMed  Google Scholar 

  • Fischer LM et al (2007) Sex and menopausal status influence human dietary requirements for the nutrient choline. Am J Clin Nutr 85:1275–1285

    PubMed Central  CAS  PubMed  Google Scholar 

  • Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Fontagne S, Geurden I, Escaffre AM, Bergot P (1998) Histological changes induced by dietary phospholipids in intestine and liver of common carp (Cyprinus carpio L.) larvae. Aquaculture 161:213–223. doi:10.1016/s0044-8486(97)00271-8

    Article  CAS  Google Scholar 

  • Food and Nutrition Board IoM (1998) Dietary Reference Intakes: thiamin, riboflavin, niacin, vitamin b-6, vitamin b-12, pantothenic acid, biotin, and choline

  • Geurden I, Radunzneto J, Bergot P (1995) Essentiality of dietary phospholipids for carp (Cyprinus carpio L.) larvae. Aquaculture 131:303–314. doi:10.1016/0044-8486(94)00344-n

    Article  CAS  Google Scholar 

  • Geurden I, Jutfelt F, Olsen RE, Sundell KS (2009) A vegetable oil feeding history affects digestibility and intestinal fatty acid uptake in juvenile rainbow trout Oncorhynchus mykiss. Comp Biochem Physiol A Mol Integr Physiol 152:552–559. doi:10.1016/j.cbpa.2008.12.016

    Article  PubMed  Google Scholar 

  • Gibellini F, Smith TK (2010) The Kennedy pathway-de novo synthesis of phosphatidylethanolamine and phosphatidylcholine. IUBMB Life 62:414–428. doi:10.1002/iub.337

    Article  CAS  PubMed  Google Scholar 

  • Hama K, Provost E, Baranowski TC, Rubinstein AL, Anderson JL, Leach SD, Farber SA (2009) In vivo imaging of zebrafish digestive organ function using multiple quenched fluorescent reporters. Am J Physiol Gastrointest Liver Physiol 296:G445–G453. doi:10.1152/ajpgi.90513.2008

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Holub BJ (1978) Differential utilization of 1-palmitoyl and 1-stearoyl homologs of various unsaturated 1,2-diacyl-sn-glycerols for phosphatidylcholine and phosphatidylethanolamine synthesis in rat-liver microsomes. J Biol Chem 253:691–696

    CAS  PubMed  Google Scholar 

  • Jin Y, Li K, Olsen Y (2014) Time kinetics of fatty acid changes in phospholipids following enrichment and starvation of Artemia franciscana with a main focus on docosahexaenoic acid. Aquac Nutr. doi:10.1111/anu.12224

    Google Scholar 

  • Jukes TH (1947) Choline. Annu Rev Biochem 16:193–222. doi:10.1146/annurev.bi.16.070147.001205

    Article  CAS  PubMed  Google Scholar 

  • Kamisaka Y, Ronnestad I (2011) Reconstructed 3D models of digestive organs of developing Atlantic cod (Gadus morhua) larvae. Mar Biol 158:233–243. doi:10.1007/s00227-010-1554-x

    Article  PubMed Central  PubMed  Google Scholar 

  • Kato T, Hayashi Y, Inoue K, Yuasa H (2005) Glycerol absorption by Na + -dependent carrier-mediated transport in the closed loop of the rat small intestine. Biol Pharm Bull 28:553–555. doi:10.1248/bpb.28.553

    Article  CAS  PubMed  Google Scholar 

  • Kent C (2005) Regulatory enzymes of phosphatidylcholine biosynthesis: a personal perspective. BBA Mol Cell Biol Lipids 1733:53–66. doi:10.1016/j.bbalip.2004.12.008

    Article  CAS  Google Scholar 

  • Kuipers F, Oude Elferink RP, Verkade HJ, Groen AK (1997) Mechanisms and (patho) physiological significance of biliary cholesterol secretion. Subcell Biochem 28:295–318

    Article  CAS  PubMed  Google Scholar 

  • Lehner R, Kuksis A (1992) Utilization of 2-monoacylglycerols for phosphatidylcholine biosynthesis in the intestine. Biochim Biophys Acta 1125:171–179. doi:10.1016/0005-2760(92)90042-t

    Article  CAS  PubMed  Google Scholar 

  • Lehner R, Kuksis A (1996) Biosynthesis of triacylglycerols. Prog Lipid Res 35:169–201. doi:10.1016/0163-7827(96)00005-7

    Article  CAS  PubMed  Google Scholar 

  • Li K, Olsen Y (2015) Effect of enrichment time and dietary DHA and non-highly unsaturated fatty acid composition on the efficiency of DHA enrichment in phospholipid of rotifer (Brachionus Cayman). Aquaculture 446:310–317. doi:10.1016/j.aquaculture.2015.05.005

    Article  CAS  Google Scholar 

  • Li ZY, Vance DE (2008) Phosphatidylcholine and choline homeostasis. J Lipid Res 49:1187–1194. doi:10.1194/jlr.R700019-JLR200

    Article  CAS  PubMed  Google Scholar 

  • Li JY, Li XF, Xu WN, Zhang CN, Liu WB (2015a) Effects of dietary choline supplementation on growth performance, lipid deposition and intestinal enzyme activities of blunt snout bream Megalobrama amblycephal fed high-lipid diet. Aquac Nutr. doi:10.1111/anu.12231

    Google Scholar 

  • Li K, Kjorsvik E, Bergvik M, Olsen Y (2015b) Manipulation of the fatty acid composition of phosphatidylcholine and phosphatidylethanolamine in rotifers Brachionus Nevada and Brachionus Cayman. Aquac Nutr 21:85–97. doi:10.1111/anu.12140

    Article  CAS  Google Scholar 

  • Li K et al (2015c) Gene regulation of lipid and phospholipid metabolism in Atlantic cod (Gadus morhua) larvae. Comp Biochem Physiol B Biochem Mol Biol. doi:10.1016/j.cbpb.2015.08.006

    Google Scholar 

  • Lynch RD (1980) Utilization of polyunsaturated fatty acids by human diploid cells aging in vitro. Lipids 15:412–420. doi:10.1007/bf02534065

    Article  CAS  PubMed  Google Scholar 

  • Mansbach CM (1977) Origin of chylomicron phosphatidylcholine in rat. J Clin Investig 60:411–420. doi:10.1172/jci108790

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mantel CR, Schulz AR, Miyazawa K, Broxmeyer HE (1993) Kinetic selectivity of cholinephosphotransferase in mouse liver: the K m for CDP-choline depends on diacylglycerol structure. Biochem J 289:815–820

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Millikin MR (1982) Qualitative and quantitative nutrient requirements of fishes: a reveiw. Fish B NOAA 80:655–686

    CAS  Google Scholar 

  • Morais S, Rojas-Garcia CR, Conceicao LEC, Ronnestad I (2005) Digestion and absorption of a pure triacylglycerol and a free fatty acid by Clupea harengus L. larvae. J Fish Biol 67:223–238. doi:10.1111/j.1095-8649.2005.00731.x

    Article  CAS  Google Scholar 

  • Morimoto K, Kanoh H (1978) Acyl chain length dependency of diacylglycerol cholinephosphotransferase and diacylglycerol ethanolaminephosphotransferase. Effect of different saturated fatty acids at the C-1 or C-2 position of diacylglycerol on solubilized rat liver microsomal enzymes. J Biol Chem 253:5056

    CAS  PubMed  Google Scholar 

  • Northfield TC, Hofmann AF (1975) Biliary lipid output during 3 meals and an overnight fast. 1. Relationship to bile acid pool size and cholesterol saturation of bile in gallstone and control subjects. Gut 16:1–12. doi:10.1136/gut.16.1.1

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ogino C, Uki N, Watanabe T, Iida Z, Ando K (1970) B vitamin requirements of carp. 4. Requirement for choline. Bull Jpn Soc Sci Fish 36:1140–1146

    Article  CAS  Google Scholar 

  • Olsen RE, Henderson RJ (1989) The rapid analysis of neutral and polar marine lipids using double-development HPTLC and scanning densitometry. J Exp Mar Biol Ecol 129:189–197. doi:10.1016/0022-0981(89)90056-7

    Article  CAS  Google Scholar 

  • Olsen RE, Myklebust R, Kaino T, Ringo E (1999) Lipid digestibility and ultrastructural changes in the enterocytes of Arctic char (Salvelinus alpinus L.) fed linseed oil and soybean lecithin. Fish Physiol Biochem 21:35–44. doi:10.1023/a:1007726615889

    Article  CAS  Google Scholar 

  • Olsen RE, Myklebust R, Ringo E, Mayhew TM (2000) The influences of dietary linseed oil and saturated fatty acids on caecal enterocytes in Arctic char (Salvelinus alpinus L.): a quantitative ultrastructural study. Fish Physiol Biochem 22:207–216. doi:10.1023/A:1007879127182

    Article  CAS  Google Scholar 

  • Olsen RE, Dragnes BT, Myklebust R, Ringo E (2003) Effect of soybean oil and soybean lecithin on intestinal lipid composition and lipid droplet accumulation of rainbow trout, Oncorhynchus mykiss Walbaum. Fish Physiol Biochem 29:181–192. doi:10.1023/b:fish.0000045708.67760.43

    Article  CAS  Google Scholar 

  • Oxley A, Torstensen BE, Rustan AC, Olsen RE (2005) Enzyme activities of intestinal triacylglycerol and phosphatidylcholine biosynthesis in Atlantic salmon (Salmo salar L.). Comp Biochem Physiol B 141:77–87. doi:10.1016/j.cbpc.2005.01.012

    Article  PubMed  Google Scholar 

  • Oxley A, Jutfelt F, Sundell K, Olsen RE (2007) Sn-2-monoacylglycerol, not glycerol, is preferentially utilised for triacylglycerol and phosphatidylcholine biosynthesis in Atlantic salmon (Salmo salar L.) intestine. Comp Biochem Physiol B 146:115–123. doi:10.1016/j.cbpb.2006.09.007

    Article  PubMed  Google Scholar 

  • Reo NV, Adinehzadeh M, Foy BD (2002) Kinetic analyses of liver phosphatidylcholine and phosphatidylethanolamine biosynthesis using C-13 NMR spectroscopy. BBA Mol Cell Biol Lipids 1580:171–188. doi:10.1016/s1388-1981(01)00202-5

    Article  CAS  Google Scholar 

  • Ronnestad I, Rojas-Garcia CR, Tonheim SK, Conceicao LEC (2001) In vivo studies of digestion and nutrient assimilation in marine fish larvae. Aquaculture 201:161–175. doi:10.1016/s0044-8486(01)00595-6

    Article  Google Scholar 

  • Rust MB, Hardy RW, Stickney RR (1993) A new method for force-feeding larval fish. Aquaculture 116:341–352. doi:10.1016/0044-8486(93)90418-x

    Article  Google Scholar 

  • Sargent JR, Tocher DR, Gordon Bell J (2002) The lipids. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd ed. Academic Press, San Diego, pp 181–257

  • Siddiqi S, Mansbach CM (2015) Dietary and biliary phosphatidylcholine activates PKC zeta in rat intestine. J Lipid Res 56:859–870. doi:10.1194/jlr.M056051

    Article  CAS  PubMed  Google Scholar 

  • Southern LL, Brown DR, Werner DD, Fox MC (1986) Excess supplemental choline for swine. J Anim Sci 62:992–996

    CAS  PubMed  Google Scholar 

  • Spector AA, John K, Fletcher JE (1969) Binding of long-chain fatty acids to bovine serum albumin. J Lipid Res 10:56–67

    CAS  PubMed  Google Scholar 

  • Star B et al (2011) The genome sequence of Atlantic cod reveals a unique immune system. Nature 477:207–210. doi:10.1038/Nature10342

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sugimoto H, Banchio C, Vance DE (2008) Transcriptional regulation of phosphatidylcholine biosynthesis. Prog Lipid Res 47:204–220. doi:10.1016/j.plipres.2008.01.002

    Article  CAS  PubMed  Google Scholar 

  • Sundler R, Akesson B (1975) Regulation of phospholipid biosynthesis in isolated rat hepatocytes-effect of different substrates. J Biol Chem 250:3359–3367

    CAS  PubMed  Google Scholar 

  • Tocher DR, Bendiksen EA, Campbell PJ, Bell JG (2008) The role of phospholipids in nutrition and metabolism of teleost fish. Aquaculture 280:21–34. doi:10.1016/j.aquaculture.2008.04.034

    Article  CAS  Google Scholar 

  • Tso P, Lam J, Simmonds WJ (1978) The importance of the lysophosphatidylcholine ad choline moiety of bile phosphatidylcholine in lymphatic transport of fat. Biochim Biophys Acta 528:364–372. doi:10.1016/0005-2760(78)90025-5

    Article  CAS  PubMed  Google Scholar 

  • Vance JE, Vance DE (2004) Phospholipid biosynthesis in mammalian cells. Biochem Cell Biol 82:113–128. doi:10.1139/003-073

    Article  CAS  PubMed  Google Scholar 

  • Yang LY, Kuksis A (1991) Apparent convergence (at 2-monoacylglycerol level) of phosphatidic acid and 2-monoacylglycerol pathways of synthesis of chylomicron triacylglycerols. J Lipid Res 32:1173–1186

    CAS  PubMed  Google Scholar 

  • Zhu J, Wu Y, Tang QY, Leng Y, Cai W (2014) The effects of choline on hepatic lipid metabolism, mitochondrial function and antioxidative status in human hepatic C3A cells exposed to excessive energy substrates. Nutrients 6:2552–2571. doi:10.3390/nu6072552

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Thanks to Dr. Peter De Schryver for his generous donation of the cod larvae. We thank the Department of Biology at NTNU for providing financial support to Keshuai Li for his PhD study (N31114).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Keshuai Li.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, K., Olsen, R.E., Østensen, MA. et al. Atlantic cod (Gadus morhua) larvae can biosynthesis phospholipid de novo from 2-oleoyl-glycerol and glycerol precursors. Fish Physiol Biochem 42, 137–147 (2016). https://doi.org/10.1007/s10695-015-0125-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-015-0125-y

Keywords

Navigation