Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
권호 표지
DOI QR코드

DOI QR Code

The dietary requirement for threonine in juvenile olive flounder (Paralichthys olivaceus)

  • Mirasha Hasanthi (Department of Marine Life Sciences, Jeju National University) ;
  • Min-Gi Kim (Department of Marine Life Sciences, Jeju National University) ;
  • Hyunwoon Lim (Department of Marine Life Sciences, Jeju National University) ;
  • Jongho Lim (Department of Marine Life Sciences, Jeju National University) ;
  • Sang-woo Hur (Aquafeed Research Center, National Institute of Fisheries Science) ;
  • Seunghan Lee (Aquafeed Research Center, National Institute of Fisheries Science) ;
  • Bong-Joo Lee (Aquafeed Research Center, National Institute of Fisheries Science) ;
  • Kang-Woong Kim (Aquafeed Research Center, National Institute of Fisheries Science) ;
  • Kyeong-Jun Lee (Department of Marine Life Sciences, Jeju National University)
  • Received : 2022.07.08
  • Accepted : 2022.11.22
  • Published : 2023.01.30
Download PDF
⟨ Previous Next ⟩

Abstract

This study was conducted to determine dietary threonine (Thr) requirement for juvenile olive flounder (Paralichthys olivaceus). A total of 450 juvenile fish (23.2 ± 0.4 g) were randomly distributed to 18 tanks (215 L) with 25 fish per tank. Experimental diets included with graded levels of Thr at 0.0%, 0.4%, 0.8%, 1.2%, 1.6%, and 2.0% were assigned for triplicate groups of fish and fed two times daily to apparent satiation for 12 weeks. Weight gain, specific growth rate, feed intake, feed utilization and survival were significantly (p < 0.05) increased in fish fed with dietary Thr levels over 0.8%, and no significant differences were observed between 0.8% to 2.3% levels. Non-specific immune parameters of serum lysozyme, myeloperoxidase activity, antiprotease activity, and total immunoglobulin were significantly increased by dietary Thr over 0.8%. Based on the broken-line regression analysis, the Thr requirement for the optimum growth and immune response in olive flounder is likely to be 1.03% in the diet.

Keywords

Acknowledgement

This research was supported by National Institute of Fisheries Science (R2022016) and Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2019R1A6A1A03033553).

References

  1. Ahmed I. Dietary amino acid L-threonine requirement of fingerling Indian catfish, Heteropneustes fossilis (Bloch) estimated by growth and biochemical parameters. Aquacult Int. 2007;15:337-50. https://doi.org/10.1007/s10499-007-9097-y
  2. Alam MS, Teshima SI, Ishikawa M, Koshio S. Methionine requirement of juvenile Japanese flounder Paralichthys olivaceus. J World Aquacult Soc. 2000;31:618-26. https://doi.org/10.1111/j.1749-7345.2000.tb00911.x
  3. Alam MS, Teshima SI, Koshio S, Ishikawa M. Arginine requirement of juvenile Japanese flounder Paralichthys olivaceus estimated by growth and biochemical parameters. Aquaculture. 2002;205:127-40. https://doi.org/10.1016/S0044-8486(01)00670-6
  4. Bartolomeo MP, Maisano F. Validation of a reversed-phase HPLC method for quantitative amino acid analysis. J Biomol Tech. 2006;17:131-7.
  5. Bodin N, Mambrini M, Wauters JB, Abboudi T, Ooghe W, Le Boulenge E, et al. Threonine requirements for rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar) at the fry stage are similar. Aquaculture. 2008;274:353-65. https://doi.org/10.1016/j.aquaculture.2007.11.031
  6. Chen YP, Cheng YF, Li XH, Yang WL, Wen C, Zhuang S, et al. Effects of threonine supplementation on the growth performance, immunity, oxidative status, intestinal integrity, and barrier function of broilers at the early age. Poult Sci. 2017;96:405-13. https://doi.org/10.3382/ps/pew240
  7. Cheng Z, Guo C, Chen Z, Yang T, Zhang J, Wang J, et al. Glycine, serine and threonine metabolism confounds efficacy of complement-mediated killing. Nat Commun. 2019;10:3325.
  8. Choi W, Hamidoghli A, Bae J, Won S, Choi YH, Kim KW, et al. On-farm evaluation of dietary animal and plant proteins to replace fishmeal in sub-adult olive flounder Paralichthys olivaceus. Fish Aquat Sci. 2020;23:22.
  9. Dabrowski K, Arslan M, Terjesen BF, Zhang Y. The effect of dietary indispensable amino acid imbalances on feed intake: is there a sensing of deficiency and neural signaling present in fish? Aquaculture. 2007;268:136-42. https://doi.org/10.1016/j.aquaculture.2007.04.065
  10. D'mello JPF. Amino acids as multifunctional molecules. Amino Acids Anim Nutr. 2003;2:1-14. https://doi.org/10.1079/9780851996547.0001
  11. Dong YW, Feng L, Jiang WD, Liu Y, Wu P, Jiang J, et al. Dietary threonine deficiency depressed the disease resistance, immune and physical barriers in the gills of juvenile grass carp (Ctenopharyngodon idella) under infection of Flavobacterium columnare. Fish Shellfish Immunol. 2018;72:161-73. https://doi.org/10.1016/j.fsi.2017.10.048
  12. Dong YW, Jiang WD, Liu Y, Wu P, Jiang J, Kuang SY, et al. Threonine deficiency decreased intestinal immunity and aggravated inflammation associated with NF-κB and target of rapamycin signalling pathways in juvenile grass carp (Ctenopharyngodon idella) after infection with Aeromonas hydrophila. Br J Nutr. 2017;118:92-108. https://doi.org/10.1017/S0007114517001830
  13. Dong YW, Jiang WD, Wu P, Liu Y, Kuang SY, Tang L, et al. Nutritional digestion and absorption, metabolism fates alteration was associated with intestinal function improvement by dietary threonine in juvenile grass carp (Ctenopharyngodon Idella). Aquaculture. 2022;555:738194.
  14. Fatma Abidi S, Khan MA. Dietary threonine requirement of fingerling Indian major carp, Labeo rohita (Hamilton). Aquacult Res. 2008;39:1498-505. https://doi.org/10.1111/j.1365-2109.2008.02018.x
  15. Feng L, Peng Y, Wu P, Hu K, Jiang WD, Liu Y, et al. Threonine affects intestinal function, protein synthesis and gene expression of TOR in Jian carp (Cyprinus carpio var. Jian). PLOS ONE. 2013;8:e69974.
  16. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226:497-509. https://doi.org/10.1016/S0021-9258(18)64849-5
  17. Forster I, Ogata HY. Lysine requirement of juvenile Japanese flounder Paralichthys olivaceus and juvenile red sea bream Pagrus major. Aquaculture. 1998;161:131-42. https://doi.org/10.1016/S0044-8486(97)00263-9
  18. Fuentes EN, Bjornsson BT, Valdes JA, Einarsdottir IE, Lorca B, Alvarez M, et al. IGF-I/PI3K/Akt and IGF-I/MAPK/ERK pathways in vivo in skeletal muscle are regulated by nutrition and contribute to somatic growth in the fine flounder. Am J Physiol Regul Integr Comp Physiol. 2011;300:R1532-42. https://doi.org/10.1152/ajpregu.00535.2010
  19. Gao YJ, Yang HJ, Liu YJ, Chen SJ, Guo DQ, Yu Y, et al. Effects of graded levels of threonine on growth performance, biochemical parameters and intestine morphology of juvenile grass carp Ctenopharyngodon idella. Aquaculture. 2014;424-5:113-9. https://doi.org/10.1016/j.aquaculture.2013.12.043
  20. Gietzen DW. Neural mechanisms in the responses to amino acid deficiency. J Nutr. 1993;123:610-25. https://doi.org/10.1093/jn/123.4.610
  21. Gietzen DW, Anthony TG, Fafournoux P, Maurin AC, Koehnle TJ, Hao S. Measuring the ability of mice to sense dietary essential amino acid deficiency: the importance of amino acid status and timing. Cell Rep. 2016;16:2049-50. https://doi.org/10.1016/j.celrep.2016.08.021
  22. Gloaguen M, Le Floc'h N, Corrent E, Primot Y, van Milgen J. Providing a diet deficient in valine but with excess leucine results in a rapid decrease in feed intake and modifies the postprandial plasma amino acid and α-keto acid concentrations in pigs. J Anim Sci. 2012;90:3135-42. https://doi.org/10.2527/jas.2011-4956
  23. Habte-Tsion HM, Ge X, Liu B, Xie J, Ren M, Zhou Q, et al. A deficiency or an excess of dietary threonine level affects weight gain, enzyme activity, immune response and immune-related gene expression in juvenile blunt snout bream (Megalobrama amblycephala). Fish Shellfish Immunol. 2015;42:439-46. https://doi.org/10.1016/j.fsi.2014.11.021
  24. Hardy RW. Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aquacult Res. 2010;41:770-6. https://doi.org/10.1111/j.1365-2109.2009.02349.x
  25. Helland SJ, Grisdale-Helland B. Replacement of fish meal with wheat gluten in diets for Atlantic halibut (Hippoglossus hippoglossus): effect on whole-body amino acid concentrations. Aquaculture. 2006;261:1363-70. https://doi.org/10.1016/j.aquaculture.2006.09.025
  26. House JD, Hall BN, Brosnan JT. Threonine metabolism in isolated rat hepatocytes. Am J Physiol Endocrinol Metab. 2001;281:E1300-7. https://doi.org/10.1152/ajpendo.2001.281.6.E1300
  27. Hultmark D, Steiner H, Rasmuson T, Boman HG. Insect immunity. Purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae of Hyalophora cecropia. Eur J Biochem. 1980;106:7-16. https://doi.org/10.1111/j.1432-1033.1980.tb05991.x
  28. Kim JM, Malintha GHT, Gunathilaka GLBE, Lee C, Kim MG, Lee BJ, et al. Taurine supplementation in diet for olive flounder at low water temperature. Fish Aquat Sci. 2017;20:20.
  29. Kim SH, Choi JH, Wang P, Go CD, Hesketh GG, Gingras AC, et al. Mitochondrial threonyl-tRNA synthetase TARS2 is required for threonine-sensitive mTORC1 activation. Mol Cell. 2021;81:398-407.E4. https://doi.org/10.1016/j.molcel.2020.11.036
  30. Kim SS, Lee KJ. Comparison of leucine requirement in olive flounder (Paralichthys olivaceus) by free or synthetic dipeptide forms of leucine. Anim Feed Sci Technol. 2013;183:195-201. https://doi.org/10.1016/j.anifeedsci.2013.05.008
  31. Koehnle TJ, Russell MC, Morin AS, Erecius LF, Gietzen DW. Diets deficient in indispensable amino acids rapidly decrease the concentration of the limiting amino acid in the anterior piriform cortex of rats. J Nutr. 2004;134:2365-71. https://doi.org/10.1093/jn/134.9.2365
  32. Konashi S, Takahashi K, Akiba Y. Effects of dietary essential amino acid deficiencies on immunological variables in broiler chickens. Br J Nutr. 2000;83:449-56.
  33. Lee CL, Li X. Serine/threonine ligation for the chemical synthesis of proteins. Curr Opin Chem Biol. 2014;22:108-14. https://doi.org/10.1016/j.cbpa.2014.09.023
  34. Li P, Mai K, Trushenski J, Wu G. New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids. 2009;37:43-53. https://doi.org/10.1007/s00726-008-0171-1
  35. Li P, Yin YL, Li D, Kim SW, Wu G. Amino acids and immune function. Br J Nutr. 2007;98:237-52. https://doi.org/10.1017/S000711450769936X
  36. Liebert F. Amino acid requirement studies in Oreochromis niloticus by application of principles of the diet dilution technique. J Anim Physiol Anim Nutr. 2009;93:787-93. https://doi.org/10.1111/j.1439-0396.2008.00869.x
  37. Liebert F, Benkendorff K. Modelling of threonine and methionine requirements of Oreochromis niloticus due to principles of the diet dilution technique. Aquacult Nutr. 2007;13:397-406. https://doi.org/10.1111/j.1365-2095.2007.00490.x
  38. Magnadottir B, Jonsdottir H, Helgason S, Bjornsson B, Jorgensen TO, Pilstrom L. Humoral immune parameters in Atlantic cod (Gadus morhua L.): I. the effects of environmental temperature. Comp Biochem Physiol B Biochem Mol Biol. 1999;122:173-80. https://doi.org/10.1016/S0305-0491(98)10156-6
  39. McAuley JL, Linden SK, Png CW, King RM, Pennington HL, Gendler SJ, et al. MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. J Clin Invest. 2007;117:2313-24. https://doi.org/10.1172/JCI26705
  40. Michelato M, Vidal LVO, Xavier TO, Graciano TS, De Moura LB, Furuya VRB, et al. Dietary threonine requirement to optimize protein retention and fillet production of fast-growing Nile tilapia. Aquacult Nutr. 2016;22:759-66. https://doi.org/10.1111/anu.12293
  41. Quade MJ, Roth JA. A rapid, direct assay to measure degranulation of bovine neutrophil primary granules. Vet Immunol Immunopathol. 1997;58:239-48. https://doi.org/10.1016/S0165-2427(97)00048-2
  42. Rahimnejad S, Lee KJ. Dietary isoleucine influences non-specific immune response in juvenile olive flounder (Paralichthys olivaceus). Turk J Fish Aquat Sci. 2014;14:853-62. https://doi.org/10.4194/1303-2712-v14_4_02
  43. Ramos-Pinto L, Manchado M, Azeredo R, Reis DB, Perez-Sanchez J, Calduch-Giner JA, et al. Short-term dietary histidine, threonine and tryptophan supplementation in fishmeal-free diets, affects immune status in gilthead seabream (Sparus aurata) juveniles [Internet]. Digital CSIC. 2017 [cited 2017 Oct 17]. http://hdl.handle.net/10261/191287
  44. Robbins KR. A method, SAS program, and example for fitting the broken-line to growth data. Knoxville: University of Tennessee; 1986. Report No.: 86-09.
  45. Ronnestad I, Kamisaka Y, Conceicao LEC, Morais S, Tonheim SK. Digestive physiology of marine fish larvae: hormonal control and processing capacity for proteins, peptides and amino acids. Aquaculture. 2007;268:82-97. https://doi.org/10.1016/j.aquaculture.2007.04.031
  46. Seiliez I, Gabillard JC, Skiba-Cassy S, Garcia-Serrana D, Gutierrez J, Kaushik S, et al. An in vivo and in vitro assessment of TOR signaling cascade in rainbow trout (Oncorhynchus mykiss). Am J Physiol Regul Integr Comp Physiol. 2008;295:R329-35. https://doi.org/10.1152/ajpregu.00146.2008
  47. Small BC, Soares JH Jr. Quantitative dietary threonine requirement of juvenile striped bass Morone saxatilis. J World Aquacult Soc. 1999;30:319-23.
  48. Tacon AGJ, Metian M. Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture. 2008;285:146-58. https://doi.org/10.1016/j.aquaculture.2008.08.015
  49. Tang Q, Tan P, Ma N, Ma X. Physiological functions of threonine in animals: beyond nutrition metabolism. Nutrients. 2021;13:2592.
  50. Uribe C, Folch H, Enriquez R, Moran G. Innate and adaptive immunity in teleost fish: a review. Vet Med. 2011;56:486-503. https://doi.org/10.17221/3294-VETMED
  51. Westerterp KR. Physical activity, food intake, and body weight regulation: insights from doubly labeled water studies. Nutr Rev. 2010;68:148-54. https://doi.org/10.1111/j.1753-4887.2010.00270.x
  52. Wilson MR, van Ravenstein E, Miller NW, Clem LW, Middleton DL, Warr GW. cDNA sequences and organization of IgM heavy chain genes in two holostean fish. Dev Comp Immunol. 1995;19:153-64. https://doi.org/10.1016/0145-305X(94)00063-L
  53. Yamamoto T, Shima T, Furuita H, Suzuki N, Sanchez-Vazquez FJ, Tabata M. Self-selection and feed consumption of diets with a complete amino acid composition and a composition deficient in either methionine or lysine by rainbow trout, Oncorhynchus mykiss (Walbaum). Aquacult Res. 2001;32:83-91. https://doi.org/10.1046/j.1355-557x.2001.00007.x
  54. Zhang Q, Chen X, Eicher SD, Ajuwon KM, Applegate TJ. Effect of threonine deficiency on intestinal integrity and immune response to feed withdrawal combined with coccidial vaccine challenge in broiler chicks. Br J Nutr. 2016;116:2030-43. https://doi.org/10.1017/S0007114516003238
  55. Zhao Y, Jiang Q, Zhou XQ, Xu SX, Feng L, Liu Y, et al. Effect of dietary threonine on growth performance and muscle growth, protein synthesis and antioxidant-related signalling pathways of hybrid catfish Pelteobagrus vachelli♀ × Leiocassis longirostris♂. Br J Nutr. 2020;123:121-34. https://doi.org/10.1017/S0007114519002599
  56. Zhou QC, Wang YL, Wang HL, Tan BP. Dietary threonine requirements of juvenile Pacific white shrimp, Litopenaeus vannamei. Aquaculture. 2013;392-395:142-7. https://doi.org/10.1016/j.aquaculture.2013.01.026