Skip to main content Accessibility help
×
Home

Modulation of selenium tissue distribution and selenoprotein expression in Atlantic salmon (Salmo salar L.) fed diets with graded levels of plant ingredients

  • Monica B. Betancor (a1), Thi M. C. Dam (a1), James Walton (a2), Thea Morken (a3), Patrick J. Campbell (a2) and Douglas R. Tocher (a1)...

Abstract

Increased substitution of marine ingredients by terrestrial plant products in aquafeeds has been proven to be suitable for Atlantic salmon farming. However, a reduction in n-3 long-chain PUFA is a consequence of this substitution. In contrast, relatively little attention has been paid to the effects of fishmeal and oil substitution on levels of micronutrients such as Se, considering fish are major sources of this mineral for human consumers. To evaluate the effects of dietary marine ingredient substitution on tissue Se distribution and the expression of Se metabolism and antioxidant enzyme genes, Atlantic salmons were fed three feeds based on commercial formulations with increasing levels of plant proteins (PP) and vegetable oil. Lipid content in flesh did not vary at any sampling point, but it was higher in the liver of 1 kg of fish fed higher PP. Fatty acid content reflected dietary input and was related to oxidation levels (thiobarbituric acid-reactive substances). Liver had the highest Se levels, followed by head kidney, whereas the lowest contents were found in brain and gill. The Se concentration of flesh decreased considerably with high levels of substitution, reducing the added value of fish consumption. Only the brain showed significant differences in glutathione peroxidase, transfer RNA selenocysteine 1-associated protein 1b and superoxide dismutase expression, whereas no significant regulation of Se-related genes was found in liver. Although Se levels in the diets satisfied the essential requirements of salmon, high PP levels led to a reduction in the supply of this essential micronutrient.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Modulation of selenium tissue distribution and selenoprotein expression in Atlantic salmon (Salmo salar L.) fed diets with graded levels of plant ingredients
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Modulation of selenium tissue distribution and selenoprotein expression in Atlantic salmon (Salmo salar L.) fed diets with graded levels of plant ingredients
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Modulation of selenium tissue distribution and selenoprotein expression in Atlantic salmon (Salmo salar L.) fed diets with graded levels of plant ingredients
      Available formats
      ×

Copyright

Corresponding author

* Corresponding author: Dr M. B. Betancor, email m.b.betancor@stir.ac.uk

References

Hide All
1. Gil, A, Serra-Majem, L, Calder, PC, et al. (2012) Systematic reviews of the role of omega-3 fatty acids in the prevention and treatment of disease. Br J Nutr 107, S1S2.
2. Campoy, C, Escolano-Margarit, V, Anjos, T, et al. (2012) Omega 3 fatty acids on child growth, visual acuity and neurodevelopment. Br J Nutr 107, S85S106.
3. Delgado-Lista, J, Perez-Martinez, P, Lopez-Miranda, J, et al. (2012) Long chain omega-3 fatty acids and cardiovascular disease: a systematic review. Br J Nutr 107, S201S213.
4. Miles, EA & Calder, PC (2012) Influence of marine n-3 polyunsaturated fatty acids on immune function and a systematic review of their effects on clinical outcomes in rheumatoid arthritis. Br J Nutr 107, S171S184.
5. Rangel-Huerta, OD, Aguilera, CM, Mesa, MD, et al. (2012) Omega-3 long-chain polyunsaturated fatty acids supplementation on inflammatory biomarkers: a systematic review of randomised clinical trials. Br J Nutr 107, S159S170.
6. Laviano, A, Rianda, S, Molfino, A, et al. (2013) Omega-3 fatty acids in cancer. Curr Opin Clin Nutr Metab Care 16, 156161.
7. Raatz, SK, Silverstein, JT, Jahns, L, et al. (2013) Issues of fish consumption for cardiovascular disease risk reduction. Nutrients 5, 10811097.
8. Fox, TE, Van den Heuvel, EG, Atherton, CA, et al. (2004) Bioavailability of selenium from fish, yeast and selenite: a comparative study in humans using stable isotopes. Eur J Clin Nutr 58, 343349.
9. Rayman, M (2011) Selenium and cancer prevention. Hered Cancer Clin Pract 10, A1.
10. European Food Safety Authority (2014) Scientific opinion on dietary reference values for selenium. EFSA J 12, 3846.
11. Bell, JG, McEvoy, J, Tocher, DR, et al. (2001) 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, 15351543.
12. Naylor, RL, Hardy, RW, Bureau, DP, et al. (2009) Feeding aquaculture in an era of finite resources. Proc Natl Acad Sci U S A 106, 1510315110.
13. Betancor, MB, Sprague, M, Sayanova, O, et al. (2015) Evaluation of a high-EPA oil from transgenic Camelina sativa in feeds for Atlantic salmon (Salmo salar L.): effects on tissue fatty acid composition, histology and gene expression. Aquaculture 444, 112.
14. Betancor, MB, Sprague, M, Usher, S, et al. (2015) A nutritionally-enhanced oil from transgenic Camelina sativa effectively replaces fish oil as a source of eicosapentaenoic acid for fish. Sci Rep 5, 8104.
15. Gatlin, DM III, Barrows, FT, Brown, P, et al. (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquacult Res 38, 551579.
16. Hartviksen, M, Bakke, AM, Vecino, JG, et al. (2014) Evaluation of the effect of commercially available plant and animal protein sources in diets for Atlantic salmon (Salmo salar L.): digestive and metabolic investigations. Fish Physiol Biochem 40, 16211637.
17. Torstensen, BE, Lie, O & Frøyland, L (2000) Lipid metabolism and tissue composition in Atlantic salmon (Salmo salar L.) – effects of capelin oil, palm oil, and oleic acid-enriched sunflower oil as dietary lipid sources. Lipids 35, 653664.
18. Rosenlund, G, Obach, A, Sandberg, MG, et al. (2001) Effect of alternative lipid sources on long-term growth performance and quality of Atlantic salmon (Salmo salar L.). Aquacult Res 32, 323328.
19. Bransden, MP, Carter, CG & Nichols, PD (2003) Replacement of fish oil with sunflower oil in feeds for Atlantic salmon (Salmo salar L.): effect on growth performance, tissue fatty acid composition and disease resistance. Comp Biochem Physiol B Biochem Mol Biol 135B, 611625.
20. Liland, NS, Rosenlund, G, Berntssen, MHG, et al. (2013) Net production of Atlantic salmon (FIFO, Fish In Fish Out<1) with dietary plant proteins and vegetable oils. Aquacult Nutr 19, 289300.
21. Mahalingam, TR, Vijayalakshmi, S, Prabhu, RK, et al. (1997) Studies on some trace and minor elements in blood. A survey of the Kalpakkam (India) population. Part III: studies on dietary intake and its correlation to blood levels. Biol Trace Elem Res 57, 223238.
22. Aro, A, Afthan, G & Varo, P (1995) Effects of supplementation of fertilizers on human selenium status in Finland. Analyst 120, 841843.
23. Alloway, BJ (2013) Bioavailability of elements in soil. In Essentials of Medical Geology: Revised Edition, pp. 351373 [O Selinus, editor]. Dordrecht: Springer Science.
24. Betancor, MB, Caballero, MJ, Terova, G, et al. (2012) Selenium inclusion decreases oxidative stress indicators and muscle injuries in sea bass larvae fed high-DHA microdiets. Br J Nutr 108, 21152128.
25. Betancor, MB, Almaida-Pagán, PF, Sprague, M, et al. (2015) Roles of selenoprotein antioxidant protection in zebrafish, Danio rerio, subjected to dietary oxidative stress. Fish Physiol Biochem 41, 705720.
26. Ribeiro, ARA, Ribeiro, L, Saele, O, et al. (2012) Iodine and selenium supplementation increased survival and changed thyroid hormone status in Senegalese sole (Solea senegalensis) larvae reared in a recirculation system. Fish Physiol Biochem 38, 725734.
27. Mariotti, M, Ridge, PC, Zhang, Y, et al. (2012) Composition and evolution of the vertebrate and mammalian selenoproteomes. PLOS ONE 7, e33066.
28. Verma, S, Hoffmann, FW, Kumar, M, et al. (2011) Selenoprotein K knockout mice exhibit deficient calcium flux in immune cells and impaired immune responses. J Immunol 186, 21272137.
29. Shchedrina, VA, Everley, RA, Zhang, Y, et al. (2011) Selenoprotein K binds multiprotein complexes and is involved in the regulation of endoplasmic reticulum homeostasis. J Biol Chem 286, 4293742948.
30. Conrad, M, Schneider, M, Seiler, A, et al. (2007) Physiological role of phospholipid hydroperoxide glutathione peroxidase in mammals. Biol Chem 388, 10191025.
31. Small-Howard, A, Morozova, N, Stoytcheva, Z, et al. (2006) Supramolecular complexes mediate selenocysteine incorporation in vivo . Mol Cell Biol 26, 22372346.
32. Herbette, S, Roeckel-Drevet, P & Drevet, JR (2007) Seleno-independent glutathione peroxidases. More than simple antioxidant scavengers. FEBS J 274, 21632180.
33. Song, JH, Fujimoto, K & Miyazawa, T (2000) Polyunsaturated (n-3) fatty acids susceptible to peroxidation are increased in plasma and tissue lipids of rats fed docosahexaenoic acid-containing oils. J Nutr 130, 30283033.
34. Rudneva, II (1997) Blood antioxidant system of Black Sea elasmobranch and teleost. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 118C, 255260.
35. Arteel, GE & Sies, H (2001) The biochemistry of selenium and the glutathione system. Environ Toxicol Pharmacol 10, 153158.
36. Association of Official Analytical Chemists (2000) Official Methods of Analysis, 17th ed. Washington, DC: AOAC International.
37. 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, 497509.
38. Christie, WW (2003) Preparation of derivatives of fatty acids. In Lipid Analysis: Isolation, Separation and Structural Analysis of Lipids, 3rd ed. pp. 205225 [WW Christie, editor]. Somerset: Oily Press.
39. 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) and cod (Gadus morhua) brains and retinas. Fish Physiol Biochem 5, 229239.
40. Burk, RF, Trumble, MJ & Lawrence, RA (1980) Rat hepatic cytosolic GSH-dependent enzyme protection against lipid peroxidation in the NADPH microsomal lipid peroxidation system. Biochim Biophys Acta 618, 3541.
41. Witting, LA & Horwitt, MK (1964) Effect of degree of fatty acid unsaturation in tocopherol deficiency-induced creatinuria. J Nutr 82, 1933.
42. Pfaffl, MW, Morgan, GW & Dempfle, L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real time PCR. Nucleic Acids Res 30, e36.
43. Menoyo, D, López-Bote, CJ, Obach, A, et al. (2005) Effect of dietary fish oil substitution with linseed oil on the performance, tissue fatty acid profile, metabolism, and oxidative stability of Atlantic salmon. J Anim Sci 83, 28532862.
44. Bendiksen, , Johnsen, CA, Olsen, HJ, et al. (2011) ) Sustainable aquafeeds: progress towards reduced reliance upon marine ingredients in diets for farmed Atlantic salmon (Salmo salar L.). Aquaculture 314, 132139.
45. Hixson, SM, Parrish, CC & Anderson, SM (2014) Full substitution of fish oil with camelina (Camelina sativa) oil, with partial substitution of fish meal with camelina meal, in diets for farmed Atlantic salmon (Salmo salar) and its effect on tissue lipids and sensory quality. Food Chem 157, 5161.
46. Fairweather-Tait, SJ, Bao, Y, Broadley, MR, et al. (2011) Selenium in human health and disease. Antioxid Redox Signal 14, 13371383.
47. Lorentzen, M, Maage, A & Julshamn, K (1994) Effects of dietary selenite or selenomethionine on tissue selenium levels of Atlantic salmon (Salmo salar). Aquaculture 121, 359367.
48. Burger, J, Jeitner, C, Donio, M, et al. (2013) Mercury and selenium levels, and selenium:mercury molar ratios of brain, muscle and other tissues in bluefish (Pomatomus saltatrix) from New Jersey, USA. Sci Total Environ 443, 278286.
49. Reiley, C (2006) Selenium in Food and Health. New York: Springer Science and Business Media.
50. Bell, JG, Tocher, DR, Henderson, RJ, et al. (2003) Altered fatty acid compositions in Atlantic salmon (Salmo salar) fed diets containing linseed and rapeseed oils can be partially restored by a subsequent fish oil finishing diet. J Nutr 133, 27932801.
51. Izquierdo, MS, Montero, D, Robaina, L, et al. (2004) Alterations in fillet fatty acid profile and flesh quality in gilthead seabream (Sparus aurata) fed vegetable oils for a long term period. Recovery of fatty acid profiles by fish oil feeding. Aquaculture 250, 431444.
52. Trushenki, JT, Lewis, HA & Kohler, CC (2008) Fatty acid profile of sunshine bass, I. Profile change is affected by initial composition and differs among tissues. Lipids 43, 629641.
53. Cotter, PA, Craig, SR & McLean, E (2008) Hyperaccumulation of selenium in hybrid striped bass: a functional food for aquaculture? Aquacult Nutr 14, 215222.
54. Küçükbay, FZ, Yazlak, H, Karaca, I, et al. (2009) The effects of dietary organic or inorganic selenium in rainbow trout (Oncorhynchus mykiss) under crowding conditions. Aquacult Nutr 15, 569576.
55. Lin, YH (2014) Effects of dietary organic and inorganic selenium on the growth, selenium concentration and meat quality of juvenile grouper Epinephelus malabaricus . Aquaculture 430, 114119.
56. Le, KT & Fotedar, R (2014) Bioavailability of selenium from different dietary sources in yellowtail kingfish (Seriola lalandi). Aquaculture 420–421, 5762.
57. National Research Council (2011) Nutrient Requirements of Fish and Shrimp. Washington, DC: The National Academies Press.
58. Burger, J & Gochfeld, M (2011) Mercury and selenium levels in 19 species of saltwater fish from New Jersey as a function of species, size, and season. Sci Total Environ 409, 14181429.
59. Oruc, EO, Sevgiler, Y & Uner, N (2004) Tissue-specific oxidative stress responses in fish exposed to 2,4-D and azinphosmethyl. Comp Biochem Physiol C Toxicol Endocrinol 137C, 4351.
60. Bell, MV & Tocher, DR (1989) Molecular species composition of the major phosphoglycerides in brain and retina from trout: occurrence of high levels of di-(n-3) polyunsaturated fatty acid species. Biochem J 264, 909915.
61. Nieminen, P, Westenius, E, Halonen, T, et al. (2014) Fatty acid composition in tissues of the farmed Siberian sturgeon (Acipenser baerii). Food Chem 159, 8084.
62. Zhang, H, Mu, Z, Xu, LM, et al. (2009) Dietary lipid level induced antioxidant response in Manchurian trout, Brachymystax lenok (Pallas) larvae. Lipids 44, 643654.
63. Pacitti, D, Lawad, MM, Sweetman, J, et al. (2015) Selenium supplementation in fish: a combined chemical and biomolecular study to understand Sel-Plex assimilation and impact on selenoproteome expression in rainbow trout (Oncorhynchus mykiss). PLOS ONE 10, e0127041.
64. Zoidis, E, Pappas, AC, Georgiou, CA, et al. (2010) Selenium affects the expression of GPX4 and catalase in the liver of chicken. Comp Biochem Physiol B Biochem Mol Biol 155B, 294300.
65. Zhang, Y, Zhou, Y, Schweizer, U, et al. (2008) Comparative analysis of selenocysteine and selenoproteome gene expression in mouse brains identifies neurons as key functional sites of selenium in mammals. J Biol Chem 283, 24272438.
66. Benner, MJ, Drew, RE, Hardy, RW, et al. (2010) Zebrafish (Danio rerio) vary by strain and sex in their behavioural and transcriptional responses to selenium supplementation. Comp Biochem Physiol A Mol Integr Physiol 157A, 310318.
67. Wahle, WK & Rotondo, D (1999) Fatty acid and endothelial cell function: regulation of adhesion molecule and redox enzyme expression. Curr Opin Clin Nutr Metab Care 2, 109115.
68. Sneddon, AA, Wu, HC, Farquharson, A, et al. (2003) Regulation of selenoprotein GPX4 expression and activity in human endothelial cells by fatty acids, cytokines and antioxidants. Atherosclerosis 171, 5765.
69. Schomburg, L & Schweizer, U (2009) Hierarchical regulation of selenoprotein expression and sex-specific effects of selenium. Biochem Biophys Acta 1790, 14531462.
70. Hesketh, J (2008) Nutrigenomics and selenium: gene expression patterns, physiological targets and genetics. Annu Rev Nutr 28, 157177.
71. Timm-Heinrich, M, Eymard, S, Baron, CP, et al. (2013) Oxidative change during ice storage of rainbow trout (Oncorhynchus mykiss) fed different ratios of marine and vegetable feed ingredients. Food Chem 136, 12201230.
72. Menoyo, D, López-Bote, CJ, Bautista, JM, et al. (2002) Herring vs. anchovy fish oils in salmon feeding. Aquat Living Resour 15, 217223.
73. Baron, CP, Svendsen, GH, Lund, I, et al. (2013) Organic plant ingredients in the diet of rainbow trout (Oncorhynchus mykiss): impact on fish muscle composition and oxidative stability. Eur J Lipid Sci Technol 115, 13671377.
74. Rayman, MP (2000) The importance of selenium to human health. Lancet 356, 233241.
75. Ministry of Agriculture, Fisheries and Food (1997) Food Surveillance Information Sheet, No. 126. Dietary Intake of Selenium. London: Joint Food Safety.

Keywords

Type Description Title
UNKNOWN
Supplementary materials

Betancor supplementary material S1
Supplementary Figure

 Unknown (64 KB)
64 KB
UNKNOWN
Supplementary materials

Betancor supplementary material S2
Supplementary Figure

 Unknown (64 KB)
64 KB

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed