Skip to main content
SpringerLink
Log in

Nutritional and environmental regulation of the synthesis of highly unsaturated fatty acids and of fatty-acid oxidation in Atlantic salmon (Salmo salar L.) enterocytes and hepatocytes

Fish Physiology and Biochemistry volume 32, pages 317–328 (2006)Cite this article

Abstract

The objective of this work was to determine whether highly unsaturated fatty acid (HUFA) synthesis and fatty-acid oxidation in Atlantic salmon (Salmo salar L.) intestine was under environmental and/or seasonal regulation. Triplicate groups of salmon were grown through a full two-year cycle on two diets containing either fish oil (FO) or a diet with 75% of the FO replaced by a vegetable oil (VO) blend containing rapeseed, palm, and linseed oils. At key points in the life cycle fatty acyl desaturation/elongation (HUFA synthesis) and oxidation activity were determined in enterocytes and hepatocytes using [1−14C]18:3n−3 as substrate. As observed previously, HUFA synthesis in hepatocytes reached a peak at seawater transfer and declined thereafter, with activity consistently greater in fish fed the VO diet. In fish fed FO, HUFA synthesis in enterocytes in the freshwater stage was at a level similar to that in hepatocytes. HUFA synthesis in enterocytes increased rapidly after seawater transfer, however, and remained high for some months after transfer before decreasing to levels that were again similar to those observed in hepatocytes. Enterocyte synthesis of HUFA was usually higher in fish fed the VO diet than in those fed the FO diet. Oxidation of [1−14C]18:3n−3 in hepatocytes from fish fed FO tended to decrease during the freshwater phase but then increased steeply, peaking just after transfer before decreasing during the remaining seawater phase. At the peak in oxidation activity around seawater transfer, activity was significantly lower in fish fed VO than in fish fed FO. In enterocytes, oxidation of [1−14C]18:3 in fish fed FO reached a peak in activity just before seawater transfer. In fish fed VO, except for high activity at nine months the pattern was similar to that obtained in enterocytes from fish fed FO, with high activity around seawater transfer and declining activity in seawater. In conclusion, fatty acid metabolism in intestinal cells seemed to be under dual nutritional and environmental or seasonal regulation. Temporal patterns of oxidation of fatty acids were usually similar in the two cell types, but HUFA synthesis in enterocytes peaked over the summer seawater phase rather than at transfer, as with hepatocytes, suggesting the possibility of different regulatory cues.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (Canada)

Fig. 1
Fig. 2 
Fig. 3
Fig. 4
Fig. 5

Abbreviations

BHT:

Butylated hydroxytoluene

FAF-BSA:

Fatty acid-free bovine serum albumin

FO:

Fish oil

HBSS:

Hanks balanced salt solution

HUFA:

Highly unsaturated fatty acids (carbon chain length ≥ C20 with ≥ 3 double bonds)

PUFA:

Polyunsaturated fatty acids

VO:

Vegetable oil

References

  • Ackman RG (1980) Fish lipids, part 1. In: Connell JJ (ed) Advances in fish science and technology. Fishing News Books, Farnham, UK, pp 87–103

    Google Scholar 

  • Agustsson T, Sundell K, Sakamoto T, Ando M, Bjornsson BT (2003) Pituitary gene expression of somatolactin, prolactin, and growth hormone during Atlantic salmon parr-smolt transformation. Aquaculture 222:229–238

    Article  CAS  Google Scholar 

  • Association of Official Analytical Chemists (1990) Official methods of analysis, vol 1, 15th edn. Association of Official Analytical Chemists, Arlington, VA, USA

  • Barlow S (2000) Fishmeal and oil: sustainable feed ingredients for aquafeeds. Global Aquacult. Advocate 4:85–88

    Google Scholar 

  • Bell MV, Dick JR (2004) Changes in the capacity to synthesise 22:6n-3 during early development in rainbow trout (Oncorhynchus mykiss). Aquaculture 235:393–409

    Article  CAS  Google Scholar 

  • Bell JG, Tocher DR, Farndale BM, Cox DI, McKinney RW, Sargent JR (1997) The effect of dietary lipid on polyunsaturated fatty acid metabolism in Atlantic salmon (Salmo salar) undergoing parr-smolt transformation. Lipids 32:515–525

    PubMed  CAS  Google Scholar 

  • Bell JG, McEvoy J, Tocher DR, McGhee F, Campbell PJ, Sargent JR (2001a) Replacement of fish oil with rapeseed oil in diets of Atlantic salmon (Salmo salar) affects tissue lipid compositions and hepatocyte fatty acid metabolism. J Nutr 131:1535–1543

    CAS  Google Scholar 

  • Bell MV, Dick JR, Porter AEA (2001b) Biosynthesis and tissue deposition of docosahexaenoic acid (22:6n-3) in rainbow trout (Oncorhynchus mykiss). Lipids 36:1153–1159

    CAS  Google Scholar 

  • Bell JG, Henderson RJ, Tocher DR, McGhee F, Dick JR, Porter A, Smullen R, Sargent JR (2002) Substituting fish oil with crude palm oil in the diet of Atlantic salmon (Salmo salar) affects tissue fatty acid compositions and hepatic fatty acid metabolism. J Nutr 132:222–230

    PubMed  CAS  Google Scholar 

  • Bell MV, Dick JR, Porter AEA (2003) Pyloric ceca are a major site of 22:6n-3 synthesis in rainbow trout (Oncorhynchus mykiss). Lipids 39:39–44

    Google Scholar 

  • Crockett EL, Sidell BD (1993) Peroxisomal β-oxidation is a significant pathway for catabolism of fatty acids in a marine teleost. Am J Physiol 264:R1004–R1009

    PubMed  CAS  Google Scholar 

  • Duston J, Saunders RL (1990) Control of the timing of smoltification in Atlantic salmon: endogenous rhythms and environmental factors. In: Saunders RL (ed) Proc. Of Canada-Norway finfish aquaculture workshop. Can. Tech. Rep. Fish. Aquat. Sci., Canada, pp 99–105

  • Fjermestadt A, Hemre GI, Holm JC, Totland GK, Frøyland L (2000) Effects of different fatty acid levels in cage-fed Atlantic mackerel (Scomber scombrus). Eur J Lipid Sci Technol 102:282–286

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Folmar LC, Dickhoff WW (1980) The parr-smolt transformation (smoltification) and seawater adaptation in salmonids: a review of selected literature. Aquaculture 21:1–37

    Article  CAS  Google Scholar 

  • Fonseca-Madrigal J, Karalazos V, Campbell PJ, Bell JG, Tocher DR (2005) Influence of dietary palm oil on growth and tissue fatty acid compositions, and fatty acid metabolism in liver and intestine in rainbow trout (Oncorhynchus mykiss). Aquacult Nutr 11:241–250

    Article  CAS  Google Scholar 

  • Frøyland L, Madsen L, Eckhoff KM, Lie Ø, Berge R (1998) Carnitine palmitoyltransferase I, carnitine palmitoyl transferase II, and acyl-CoA oxidase activities in Atlantic salmon (Salmo salar). Lipids 33:923–930

    PubMed  Google Scholar 

  • Frøyland L, Lie Ø, Berge RK (2000) Mitochondrial and peroxisomal beta-oxidation capacities in various tissues from Atlantic salmon Salmo salar. Aquacult Nutr 6:85–89

    Article  Google Scholar 

  • Ghioni C, Tocher DR, Sargent JR (1997) The effect of culture on morphology, lipid and fatty acid composition, and polyunsaturated fatty acid metabolism of rainbow trout (Oncorhynchus mykiss) skin cells. Fish Physiol Biochem 16:499–513

    Article  CAS  Google Scholar 

  • Gillespie JM, Roy D, Cui H, Belsham DD (2004) Repression of gonadotropin-releasing hormone (GnRH) gene expression by melatonin may involve transcription factors COUP-TFI and C/EBPb binding at the GnRH enhancer. Neuroendocrinology 79:63–72

    Article  PubMed  CAS  Google Scholar 

  • Henderson RJ (1996) Fatty acid metabolism in freshwater fish with particular reference to polyunsaturated fatty acids. Arch Anim Nutr 49:5–22

    Article  CAS  Google Scholar 

  • Henderson RJ, Sargent JR (1985) Chain length specificities of mitochondrial and peroxisomal β-oxidation of fatty acids in rainbow trout (Salmo gairdneri). Comp Biochem Physiol 82B:79–85

    CAS  Google Scholar 

  • Jump DB, Thelen A, Ren B, Mater M (1999) Multiple mechanisms for polyunsaturated fatty acid regulation of hepatic gene transcription. Prostaglandins Leukot Essent Fatty Acids 60:345–349

    Article  PubMed  CAS  Google Scholar 

  • Kiessling K-H, Kiessling A (1993) Selective utilisation of fatty acids in rainbow trout (Oncorhynchus mykiss, Walbaum) red muscle mitochondria. Can J Zool 71:248–251

    CAS  Google Scholar 

  • Li H-O, Yamada J (1992) Changes of the fatty acid composition in smolts of masu salmon (Oncoryhnchus masou) associated with desmoltification and seawater transfer. Comp Biochem Physiol 103A:221–226

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Nakamura MT, Nara TY (2004) Structure, function, and dietary regulation of Δ6, Δ5 and Δ9 desaturases. Ann Rev Nutr 24:345–376

    Article  CAS  Google Scholar 

  • Nanton DA, Lall SP, Ross NW, McNiven MA (2003) Effect of dietary lipid level on fatty acid β-oxidation and lipid composition in various tissues of haddock, Melanogrammus aeglefinus L. Comp Biochem Physiol 135B:95–108

    CAS  Google Scholar 

  • National Research Council (1993) Nutrient requirements of fish. National Academy Press, Washington DC, USA

    Google Scholar 

  • Oxley A, Tocher DR, Torstensen BE, Olsen RE (2005) Fatty acid utilization and metabolism in caecal enterocytes from rainbow trout (Oncorhynchus mykiss L.) fed dietary fish or copepod oil. Biochim Biophys Acta 1737:119–129

    PubMed  CAS  Google Scholar 

  • Pike I (2005) Eco-efficiency in aquaculture: global catch of wild fish used in aquaculture. Int Aquafeed 8:38–40

    Google Scholar 

  • Sargent JR, Tacon A (1999) Development of farmed fish: a nutritionally necessary alternative to meat. Proc Nutr Soc 58:377–383

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Sheridan MA, Allen WV, Kerstetter TH (1985) Changes in the fatty acid composition of steelhead trout, Salmo gairdnerii Richardson associated with parr-smolt transformation. Comp Biochem Physiol 80B:671–676

    CAS  Google Scholar 

  • Stubhaug I, Lie Ø, Torstensen BE (2005a) ®-oxidation capacity in tissues of Atlantic salmon (Salmo salar L.) during smoltification, fed either 100% capelin oil or 100% vegetable oil blend. J Fish Biol 69:504–517

    Article  CAS  Google Scholar 

  • Stubhaug I, Frøyland L, Torstensen BE (2005b) β-oxidation capacity of red and white muscle and liver in Atlantic salmon (Salmo salar L.) - effects of increasing dietary levels of rapeseed oil and olive oil to replace capelin oil. Lipids 40:39–47

    CAS  Google Scholar 

  • Stubhaug I, Tocher DR, Bell JG, Dick JR, Torstensen BE (2005c) Fatty acid metabolism in Atlantic salmon (Salmo salar L.) hepatocytes, and influence of dietary vegetable oil. Biochim Biophys Acta 1734:277–288

    CAS  Google Scholar 

  • Stubhaug I, Lie Ø, Torstensen BE (2006) Fatty acid productive value and β-oxidation capacity in Atlantic salmon (Salmo salar L.) fed different lipid sources along the whole growth period. Aquacult Nutr In press

  • Tacon AGJ (2004) Use of fish meal and fish oil in aquaculture: a global perspective. Aquat Resour Cult Dev 1:3–14

    Article  Google Scholar 

  • Tidwell JH, Allan GL (2002) Fish as food: aquaculture’s contribution. World Aquacult 33:44–48

    Google Scholar 

  • Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184

    CAS  Google Scholar 

  • Tocher DR, Harvie DG (1988) Fatty acid compositions of the major phosphoglycerides from fish neural tissues : (n-3) and (n-6) polyunsaturated fatty acids in rainbow trout (Salmo gairdneri, L.) and cod (Gadus morhua) brains and retinas. Fish Physiol Biochem 5:229–239

    Article  CAS  Google Scholar 

  • Tocher DR, Bell JG, Henderson RJ, McGhee F, Mitchell D, Morris PC (2000) The effect of dietary linseed and rapeseed oils on polyunsaturated fatty acid metabolism in Atlantic salmon (Salmo salar) undergoing parr-smolt transformation. Fish Physiol Biochem 23:59–73

    Article  CAS  Google Scholar 

  • Tocher DR, Fonseca-Madrigal J, Bell JG, Dick JR, Henderson RJ, Sargent JR (2002) Effects of diets containing linseed oil on fatty acid desaturation and oxidation in hepatocytes and intestinal enterocytes in Atlantic salmon (Salmo salar). Fish Physiol Biochem 26:157–170

    Article  CAS  Google Scholar 

  • Tocher DR, Bell JG, McGhee F, Dick JR, Fonseca-Madrigal J (2003) Effects of dietary lipid level and vegetable oil on fatty acid metabolism in Atlantic salmon (Salmo salar) over the entire production cycle. Fish Physiol Biochem 29:193–209

    Article  CAS  Google Scholar 

  • Tocher DR, Fonseca-Madrigal J, Dick JR, Ng W-K, Bell JG, Campbell PJ (2004) Effects of diets containing crude palm oil and water temperature on fatty acid desaturation and oxidation in hepatocytes and intestinal enterocytes in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol 137B:49–63

    CAS  Google Scholar 

  • Torstensen BE, Li Ø, Frøyland L (2000) Lipid metabolism and tissue composition in Atlantic salmon (Salmo salar L.) – effects of capelin-, palm- and oleic acid enriched sunflower oil as dietary lipid sources. Lipids 35:653–664

    PubMed  CAS  Google Scholar 

  • U.S. National Research Council (1993) Nutrient requirements of fish. National Academy Press, Washington DC

    Google Scholar 

  • Vegusdal A, Ostbye TK, Tran TN, Gjøen T, Ruyter B (2004) β-Oxidation, esterification, and secretion of radiolabeled fatty acids in cultivated Atlantic salmon skeletal muscle cells. Lipids 39:649–658

    PubMed  CAS  Google Scholar 

  • Wedermeyer GA, Saunders RL, Clarke WC (1980) Environmental factors affecting smoltification and early marine survival of anadromous salmonids. Mar Fish Rev 42:1–14

    Google Scholar 

  • Wilson R, Sargent JR (1992) High resolution separation of polyunsaturated fatty acids by argentation thin-layer chromatography. J Chromatogr 623:403–407

    Article  CAS  Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice-Hall, Englewood Cliffs

  • Zheng X, Tocher DR, Dickson CA, Bell JG, Teale AJ (2004) Effects of diets containing vegetable oil on expression of genes involved in polyunsaturated fatty acid biosynthesis in liver of Atlantic salmon (Salmo salar). Aquaculture 236:467–483

    Article  CAS  Google Scholar 

  • Zheng X, Torstensen B, Tocher DR, Dick JR, Henderson RJ, Bell JG (2005) Environmental and dietary influences on highly unsaturated fatty acid biosynthesis and expression of fatty acyl desaturase and elongase genes in liver of Atlantic salmon (Salmo salar). Biochim Biophys Acta 1734:13–24

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported in part by the European Union (Researching alternatives to fish oils in aquaculture, RAFOA, QLRT-2000-30058) as part of the Fifth Framework Programme. JFM was supported by a studentship award from the National Council for Science and Technology (CONACyT), Mexico.

Author information

Authors and Affiliations

  1. Institute of Aquaculture, University of Stirling, Stirling, FK9 4LA, Scotland

    Jorge Fonseca-Madrigal, J. Gordon Bell & Douglas R. Tocher

Authors
  1. Jorge Fonseca-Madrigal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Gordon Bell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Douglas R. Tocher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Douglas R. Tocher.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Fonseca-Madrigal, J., Bell, J.G. & Tocher, D.R. Nutritional and environmental regulation of the synthesis of highly unsaturated fatty acids and of fatty-acid oxidation in Atlantic salmon (Salmo salar L.) enterocytes and hepatocytes. Fish Physiol Biochem 32, 317–328 (2006). https://doi.org/10.1007/s10695-006-9109-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-006-9109-2

Keywords

  • Atlantic salmon
  • Life cycle
  • Enterocytes
  • Hepatocytes
  • PUFA
  • HUFA
  • Desaturation/elongation
  • β-Oxidation
  • Vegetable oil

Search

Navigation