Effects of dietary glutamate and succinate on growth performance and mitochondrial respiration in heart and liver of Atlantic salmon (Salmo salar) smolts

Manoharan  Naveenan; Rolf Erik  Olsen; Bjørg  Egelandsdal

doi:10.17017/j.fish.2

Manoharan Naveenan Department of Biology, Faculty of Natural Sciences, Norwegian University of Science and Technology, Trondheim, Norway
Rolf Erik Olsen Department of Biology, Faculty of Natural Sciences, Norwegian University of Science and Technology, Trondheim, Norway
Bjørg Egelandsdal Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås, Norway

Keywords: Atlantic salmon, mitochondria, succinate, glutamate, respiration, high resolution respirometry

Abstract

The smolt stage of salmon has challenges in reaching adequate growth rates due to the changing environmental conditions at sea. Therefore, it is necessary to provide adequate diets to achieve sufficient growth. This study determined the impacts of glutamate and succinate (1% each) supplemented diet on the growth of Atlantic salmon smolts along with characterization of mitochondrial respiration using high-resolution respirometry technique. Results indicated that there was no significant difference in growth response between the treatment and control groups. Maximum oxidative phosphorylation (OXPHOS) was reached after addition of succinate. Analysis of heart homogenates revealed a significant difference in LEAK respiration state (P = 0.005). No significant difference was recorded between the diet groups for liver homogenates. Differences between heart and liver respiration revealed that mitochondrial activity is organ dependent.

References

Alne H, Oehme M, Thomassen M, Terjesen B and Rørvik K-A (2011) Reduced growth, condition factor and body energy levels in Atlantic salmon Salmo salar L. during their first spring in the sea. Aquaculture Research 42(2): 248–259.

Alne H, Thomassen MS, Takle H, Terjesen BF, Grammes F, Oehme M, Refstie S, Sigholt T, Berge RK and Rørvik KA (2009) Increased survival by feeding tetradecylthioacetic acid during a natural outbreak of heart and skeletal muscle inflammation in S0 Atlantic salmon, Salmo salar L. Journal of Fish Diseases 32: 953–961.

Brandt M (2010) Introduction to Absorbance Spectroscopy. https://www.rose-hulman.edu/~brandt/Fluorescence/Absorbance_Spectroscopy.pdf (accessed on 24 April 2018).

Brosnan JT (2000) Glutamate, at the interface between amino acid and carbohydrate metabolism. The Journal of Nutrition 130(4S Suppl): 988s–990s.

Burrells C, Williams PD and Forno PF (2001) Dietary nucleotides: a novel supplement in fish feeds 1. Effects on resistance to disease in salmonids. Aquaculture 199: 159–169.

Cheng Z, Buentello A and Gatlin DM (2011) Effects of dietary arginine and glutamine on growth performance, immune responses and intestinal structure of red drum, Sciaenops ocellatus. Aquaculture 319: 247–252.

Eigentler A, Draxl A, Wiethüchter A, Kuznetsov A V, Lassing B and Gnaiger E (2015) Laboratory protocol: citrate synthase a mitochondrial marker enzyme. Mitochondrial Physiology Network 17.04(03): 1–11.

FAO (2005) National Aquaculture Sector Overview - Norway. http://www.fao.org/fishery/countrysector/naso_norway/en. Accessed on 5 September 2018.

FAO (2018) The State of World Fisheries and Aquaculture- Meeting the Sustainable Development Goals. Food and Agriculture Organization of the United Nations, Rome, Italy.

Fasching M and Gnaiger E (2016) O2k quality control 2: instrumental oxygen background correction and accuracy of oxygen flux. http://wiki.oroboros.at/index.php/ MiPNet14.06_Instrumentalo2Background (accessed on 22 May 2018).

Fasching M, Fontana-Ayoub M and Gnaiger E (2016) Mitochondrial respiration medium - MiR06. www.bioblast.at/index.php/MiPNet14.13_Medium-MiR06 (accessed on 15 February 2018).

Gnaiger E (2009) Capacity of oxidative phosphorylation in human skeletal muscle: new perspectives of mitochondrial physiology. The International Journal of Biochemistry and Cell Biology 41(10): 1837–1845.

Hasli PR (2015) Characterization of mitochondrial respiration and quality differences in diploid and triploid Atlantic salmon (Salmo salar L.) at 5°C, 10°C and 15°C. MSc thesis, Norwegian University of Life Sciences, Ås, Norway.

Kolarevic J, Takle H, Felip O, Ytteborg E, Selset R, Good CM, Baeverfjord G, Asgard T and Terjesen BF (2012) Molecular and physiological responses to long-term sublethal ammonia exposure in Atlantic salmon (Salmo salar). Aquatic Toxicology 124–125: 48–57.

Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R and Kunz WS (2008) Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nature Protocols 3(6): 965–976.

Larsson T, Koppang EO, Espe M, Terjesen BF, Krasnov A, Moreno HM, Rørvik K-A, Thomassen M and Mørkøre T (2014) Fillet quality and health of Atlantic salmon (Salmo salar L.) fed a diet supplemented with glutamate. Aquaculture 426–427: 288–295.

Li P, Mai K, Trushenski J and Wu G (2009) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37(1): 43–53.

Lugert V, Thaller G, Tetens J, Schulz C and Krieter J (2016) A review on fish growth calculation: multiple functions in fish production and their specific application. Reviews in Aquaculture 8(1): 30–42.

Meijer AJ (2003) Amino Acids as Regulators and Components of Nonproteinogenic Pathways. The Journal of Nutrition 133(6): 2057S–2062S.

Minarik P, Tomaskova N, Kollarova M and Antalik M (2002) Malate dehydrogenases--structure and function. General physiology & biophysics 21(3): 257–265.

Moriyama T and Srere PA (1971) Purification of Rat Heart and Rat Liver Citrate Synthases. The Journal of Biological Chemistry 246(10): 3217–3223.

Neu J, Shenoy V and Chakrabarti R (1996) Glutamine nutrition and metabolism: where do we go from here? The FASEB Journal 10(8): 829–837.

Oehme M, Grammes F, Takle H, Zambonino-Infante J-L, Refstie S, Thomassen MS, Rørvik K-A and Terjesen BF (2010) Dietary supplementation of glutamate and arginine to Atlantic salmon (Salmo salar L.) increases growth during the first autumn in sea. Aquaculture 310: 156–163.

Rørvik K-A, Alne H, Gaarder M, Ruyter B, Måseide NP, Jakobsen JV, Berge RK, Sigholt T and Thomassen MS (2007) Does the capacity for energy utilization affect the survival of post-smolt Atlantic salmon, Salmo salar L., during natural outbreaks of infectious pancreatic necrosis. Journal of Fish Diseases 30: 399–409.

Shepherd D and Garland PB (1969) The kinetic properties of citrate synthase from rat liver mitochondria. Biochemical Journal 114(3): 597–610.

Tapiero H, Mathe G, Couvreur P and Tew KD (2002) II. Glutamine and glutamate. Biomedicine & pharmacotherapy 56(9): 446–457.

Thorpe JE, Adams CE, Miles MS and Keay DS (1989) Some influences of photoperiod and temperature on opportunity for growth in juvenile Atlantic salmon, Salmo salar L. Aquaculture 82(1): 119–126.

Trichet VV (2010) Nutrition and immunity: an update. Aquaculture Research 41(3): 356–372.

Vadder FD, Kovatcheva-Datchary P, Zitoun C, Duchampt A, Backhed F and Mithieux G (2016) Microbiota-produced succinate improves glucose homeostasis via intestinal gluconeogenesis. Cell Metabolism 24: 151–157.

Walker JM (2002) The protein protocols handbook. Humana Press, Totowa, NJ.