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Adequate supply of dietary taurine stimulates expression of molecular markers of growth and protein turnover in juvenile barramundi (Lates calcarifer)

  • David A. PoppiEmail author
  • Stephen S. Moore
  • Nicholas M. Wade
  • Brett D. Glencross
Article

Abstract

A trial was conducted to investigate the effect of dietary taurine (Tau) supply on the plasma amino acid composition and hepatic expression of several genes in juvenile barramundi (Lates calcarifer) after feeding. Triplicate tanks of fish (average weight, 89.3 g) were fed diets containing either a deficient (1 g kg−1), adequate (8 g kg−1) or excessive (19 g kg−1) level of dietary Tau. Liver tissues collected before feeding, and at 2- and 4-h post-feeding, were analysed for expression of genes involved in pathways of sulphur amino acid turnover, Tau biosynthesis and transport, target of rapamycin (TOR) signalling, the somatotropic axis and protein turnover. The treatment had no significant effect on the profiles of any amino acid in plasma collected over time after feeding, other than Tau and glycine. The expression profile of cystine and Tau synthetic genes suggested an effect of Tau excess on the metabolism of cystine. Markers of two pathways of Tau biosynthesis appear to be active in this species, providing proof that this species possesses the ability to synthesise Tau from SAA precursors. A marker for the regulation of Tau transport and homeostasis was shown to be directly regulated by Tau availability, whilst a link between adequate supply of Tau and TOR pathway-mediated growth stimulation was also apparent. An observed depression in expression of genes of the somatotropic axis, coupled with upregulation of the proteolytic and TOR-suppressing genes, in response to excessive Tau supply in the diet, signalled that excessive Tau may not be conducive to optimal growth in this species.

Keywords

Barramundi Lates calcarifer Taurine Post-prandial Protein turnover 

Notes

Acknowledgements

The authors wish to acknowledge the staff of the CSIRO Bribie Island Aquaculture Centre (BIRC): Mr. Simon Irvin, Ms. Natalie Habilay, Mr. Isaak Kadel and Mr. Joel Slinger for their assistance in the collection of samples and Mr. David Blyth in the preparation of the diets.

Funding information

This research did not receive a specific grant but was funded by the Commonwealth Scientific and Industrial Research Organisation (CSIRO) and The Queensland Alliance for Agriculture and Food Innovation. David Poppi received support through an Australian Government Research Training Program Scholarship.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Alam M, Teshima S, Koshio S, Ishikawa M (2004) Effects of supplementation of coated crystalline amino acids on growth performance and body composition of juvenile kuruma shrimp Marsupenaeus japonicus. Aquac Nutr 10:309–316CrossRefGoogle Scholar
  2. Al-Feky SSA, El-Sayed AFM, Ezzat AA (2016a) Dietary taurine improves reproductive performance of Nile tilapia (Oreochromis niloticus) broodstock. Aquac Nutr 22:392–399CrossRefGoogle Scholar
  3. Al-Feky SSA, El-Sayed AFM, Ezzat AA (2016b) Dietary taurine enhances growth and feed utilization in larval Nile tilapia (Oreochromis niloticus) fed soybean meal-based diets. Aquac Nutr 22:457–464CrossRefGoogle Scholar
  4. Asha K, Devadasan K (2013) Protective effect of taurine on the mitochondria of albino rats induced with fulminant hepatic failure. Biomed Prev Nutr 3:279–283CrossRefGoogle Scholar
  5. Belghit I, Skiba-Cassy S, Geurden I, Dias K, Surget A, Kaushik S, Panserat S, Seiliez I (2014) Dietary methionine availability affects the main factors involved in muscle protein turnover in rainbow trout (Oncorhynchus mykiss). Br J Nutr 112(4):493–503PubMedCrossRefPubMedCentralGoogle Scholar
  6. Chatzifotis S, Polemitou I, Divanach P, Antonopoulou E (2008) Effect of dietary taurine supplementation on growth performance and bile salt activated lipase activity of common dentex, Dentex dentex, fed a fish meal/soy protein concentrate-based diet. Aquaculture 275:201–208CrossRefGoogle Scholar
  7. Clemmons DR, Underwood LE (1991) Nutritional regulation of IGF-I and IGF binding proteins. Annu Rev Nutr 11:393–412PubMedCrossRefPubMedCentralGoogle Scholar
  8. Davey JF, Ersser RS (1990) Amino acid analysis of physiological fluids by high-performance liquid chromatography with phenylisothiocyanate derivatization and comparison with ion-exchange chromatography. J Chromatogr B Biomed Sci Appl 528:9–23CrossRefGoogle Scholar
  9. de Moura LB, Diógenes AF, Campelo DAV, de Almeida FLA, Pousão-Ferreira PM, Furuya WM, Peres H, Oliva-Teles A (2019) Nutrient digestibility, digestive enzymes activity, bile drainage alterations and plasma metabolites of meagre (Argyrosomus regius) feed high plant protein diets supplemented with taurine and methionine. Aquaculture 511:734231CrossRefGoogle Scholar
  10. De Santis C, Smith-Keune C, Jerry DR (2011) Normalizing RT-qPCR data: are we getting the right answers? An appraisal of normalization approaches and internal reference genes from a case study in the finfish Lates calcarifer. Mar Biotechnol 13:170–180PubMedCrossRefPubMedCentralGoogle Scholar
  11. El-Sayed AFM (2014) Is dietary taurine supplementation beneficial for farmed fish and shrimp? A comprehensive review. Rev Aquac 6:241–255CrossRefGoogle Scholar
  12. Espe M, Ruohonen K, El-Mowafi A (2012) Effect of taurine supplementation on the metabolism and body lipid-to-protein ratio in juvenile Atlantic salmon (Salmo salar). Aquac Res 43:349–360CrossRefGoogle Scholar
  13. Gabillard JC, Kamangar BB, Montserrat N (2006) Coordinated regulation of the GH/IGF system genes during refeeding in rainbow trout (Oncorhynchus mykiss). J Endocrinol 191:15–24PubMedCrossRefPubMedCentralGoogle Scholar
  14. Glencross B, Wade N, Morton K (2013) Lates calcarifer nutrition and feeding practices. In: Jerry DR (ed) Biology and culture of Asian seabass Lates Calcarifer. CRC Press, Boca Raton, pp 178–228Google Scholar
  15. Glencross B, Blyth D, Irvin S, Bourne N, Campet M, Boisot P, Wade NM (2016) An evaluation of the complete replacement of both fishmeal and fish oil in diets for juvenile Asian seabass, Lates calcarifer. Aquaculture 451:298–309CrossRefGoogle Scholar
  16. Gómez-Requeni P, Mingarro M, Kirchner S, Calduch-Giner J, Médale F, Corraze G, Panserat S, Martin S, Houlihan D, Kaushik S (2003) Effects of dietary amino acid profile on growth performance, key metabolic enzymes and somatotropic axis responsiveness of gilthead sea bream (Sparus aurata). Aquaculture 220:749–767CrossRefGoogle Scholar
  17. Green M, Sambrook J (2012) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  18. Hevrøy E, El-Mowafi A, Taylor R, Olsvik P, Norberg B, Espe M (2007) Lysine intake affects gene expression of anabolic hormones in Atlantic salmon, Salmo salar. Gen Comp Endocrinol 152:39–46PubMedCrossRefPubMedCentralGoogle Scholar
  19. Hook SE, Kroon FJ, Metcalfe S, Greenfield PA, Moncuquet P, McGrath A, Smith R, Warne MSJ, Turner RD, McKeown A (2017) Global transcriptomic profiling in barramundi (Lates calcarifer) from rivers impacted by differing agricultural land uses. Environ Toxicol Chem 36:103–112PubMedCrossRefPubMedCentralGoogle Scholar
  20. Huang K-H, Chang C-C, Ho J-D, Lu R-H, Tsai LH (2011) Role of taurine on acid secretion in the rat stomach. J Biomed Sci 18:1CrossRefGoogle Scholar
  21. Huxtable R (1992) Physiological actions of taurine. Physiol Rev 72:101–163PubMedCrossRefPubMedCentralGoogle Scholar
  22. Jia P, Xue M, Zhu X, Liu H-Y, Wu X-F, Wang J, Zheng Y-HA, Xu M (2013) Effects of dietary methionine levels on the growth performance of juvenile gibel carp (Caeassius auratus gibelio). Acta Hydrobiol Sin 37:217–226Google Scholar
  23. Kaushik SJ, Seiliez I (2010) Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs. Aquac Res 41:322–332CrossRefGoogle Scholar
  24. Kim SK, Matsunari H, Nomura K, Tanaka H, Yokoyama M, Murata Y, Ishihara K, Takeuchi T (2008) Effect of dietary taurine and lipid contents on conjugated bile acid composition and growth performance of juvenile Japanese flounder Paralichthys olivaceus. Fish Sci 74:875–881CrossRefGoogle Scholar
  25. Kim YS, Sasaki T, Awa M, Inomata M, Honryo T, Agawa Y, Ando M, Sawada Y (2016) Effect of dietary taurine enhancement on growth and development in red sea bream Pagrus major larvae. Aquac Res 47:1168–1179CrossRefGoogle Scholar
  26. Kwasek K, Terova G, Lee BJ, Bossi E, Saroglia M, Dabrowski K (2014) Dietary methionine supplementation alters the expression of genes involved in methionine metabolism in salmonids. Aquaculture 433:223–228CrossRefGoogle Scholar
  27. Lahnsteiner F, Caberlotto S (2012) Motility of gilthead seabream Sparus aurata spermatozoa and its relation to temperature, energy metabolism and oxidative stress. Aquaculture 370:76–83CrossRefGoogle Scholar
  28. Lansard M, Panserat S, Plagnes-Juan E, Seiliez I, Skiba-Cassy S (2010) Integration of insulin and amino acid signals that regulate hepatic metabolism-related gene expression in rainbow trout: role of TOR. Amino Acids 39:801–810PubMedCrossRefPubMedCentralGoogle Scholar
  29. Li P, Mai K, Trushenski J, Wu G (2009) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37:43–53PubMedCrossRefPubMedCentralGoogle Scholar
  30. Li M, Lai H, Li Q, Gong S, Wang R (2016) Effects of dietary taurine on growth, immunity and hyperammonemia in juvenile yellow catfish Pelteobagrus fulvidraco fed all-plant protein diets. Aquaculture 450:349–355CrossRefGoogle Scholar
  31. Liang H, Ren M, Habte-Tsion HM, Ge X, Xie J, Mi H, Xi B, Miao L, Liu B, Zhou Q, Fang W (2016) Dietary arginine affects growth performance, plasma amino acid contents and gene expressions of the TOR signaling pathway in juvenile blunt snout bream, Megalobrama amblycephala. Aquaculture 461:1–8CrossRefGoogle Scholar
  32. Marshall OJ (2004) PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 20:2471–2472CrossRefGoogle Scholar
  33. Martins N, Estevão-Rodrigues T, Diógenes AF, Diaz-Rosales P, Oliva-Teles A, Peres H (2018) Taurine requirement for growth and nitrogen accretion of European sea bass (Dicentrarchus labrax, L.) juveniles. Aquaculture 494:19–25CrossRefGoogle Scholar
  34. McGoogan B, Gatlin D (1997) Effects of replacing fish meal with soybean meal in diets for red drum Sciaenops ocellatus and potential for palatability enhancement. J World Aquacult Soc 28:374–385CrossRefGoogle Scholar
  35. Panserat S, Kaushik SJ (2010) Regulation of gene expression by nutritional factors in fish. Aquac Res 41:751–762CrossRefGoogle Scholar
  36. Pierce AL, Breves JP, Moriyama S, Uchida K, Grau EG (2012) Regulation of growth hormone (GH) receptor (GHR1 and GHR2) mRNA level by GH and metabolic hormones in primary cultured tilapia hepatocytes. Gen Comp Endocrinol 179:22–29PubMedCrossRefPubMedCentralGoogle Scholar
  37. Pinto W, Figueira L, Santos A, Barr Y, Helland S, Dinis MT, Aragão C (2013) Is dietary taurine supplementation beneficial for gilthead seabream (Sparus aurata) larvae? Aquaculture 384-387:1–5CrossRefGoogle Scholar
  38. Poppi DA, Moore SS, Glencross BD (2017) Redefining the requirement for total sulfur amino acids in the diet of barramundi (Lates calcarifer) including assessment of the cystine replacement value. Aquaculture 471:213–222CrossRefGoogle Scholar
  39. Poppi DA, Glencross BD, Moore SS (2018) The effect of taurine supplementation to a plant-based diet for barramundi (Lates calcarifer) with varying methionine content. Aquac Nutr 24:1340–1350.  https://doi.org/10.1111/anu.12671 CrossRefGoogle Scholar
  40. Poppi DA, Moore SS, Wade NM, Glencross BD (2019) Postprandial plasma free amino acid profile and hepatic gene expression in juvenile barramundi (Lates calcarifer) is more responsive to feed consumption than to dietary methionine inclusion. Aquaculture 501:345–358.  https://doi.org/10.1016/j.aquaculture.2018.11.044 CrossRefGoogle Scholar
  41. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna http://www.R-project.org/ Google Scholar
  42. Resuehr D, Spiess A-N (2003) A real-time polymerase chain reaction-based evaluation of cDNA synthesis priming methods. Anal Biochem 322:287–291PubMedCrossRefPubMedCentralGoogle Scholar
  43. Ripps H, Shen W (2011) Review: Taurine: a “very essential” amino acid. Mol Vis 18:2673–2686Google Scholar
  44. Rolland M, Dalsgaard J, Holm J, Gómez-Requeni P, Skov PV (2015) Dietary methionine level affects growth performance and hepatic gene expression of GH–IGF system and protein turnover regulators in rainbow trout (Oncorhynchus mykiss) fed plant protein-based diets. Comp Biochem Physiol B: Biochem Mol Biol 181:33–41CrossRefGoogle Scholar
  45. Salini MJ, Turchini GM, Wade NM, Glencross BD (2015) Rapid effects of essential fatty acid deficiency on growth and development parameters and transcription of key fatty acid metabolism genes in juvenile barramundi (Lates calcarifer). Br J Nutr 114:1784–1796PubMedCrossRefPubMedCentralGoogle Scholar
  46. Salze GP, Davis DA (2015) Taurine: a critical nutrient for future fish feeds. Aquaculture 437:215–229CrossRefGoogle Scholar
  47. Salze G, McLean E, Craig SR (2012) Dietary taurine enhances growth and digestive enzyme activities in larval cobia. Aquaculture 362:44–49CrossRefGoogle Scholar
  48. Satriyo TB, Galaviz MA, Salze G, López LM (2017) Assessment of dietary taurine essentiality on the physiological state of juvenile Totoaba macdonaldi. Aquac Res 48:5677–5689CrossRefGoogle Scholar
  49. Schuller-Levis GB, Park E (2003) Taurine: new implications for an old amino acid. FEMS Microbiol Lett 226:195–202PubMedCrossRefPubMedCentralGoogle Scholar
  50. Takagi S, Murata H, Goto T, Endo M, Yamashita H, Ukawa M (2008) Taurine is an essential nutrient for yellowtail Seriola quinqueradiata fed non-fish meal diets based on soy protein concentrate. Aquaculture 280:198–205CrossRefGoogle Scholar
  51. Takagi S, Murata H, Goto T, Hatate H, Endo M, Yamashita H, Miyatake H, Ukawa M (2010) Necessity of dietary taurine supplementation for preventing green liver symptom and improving growth performance in yearling red sea bream Pagrus major fed nonfishmeal diets based on soy protein concentrate. Fish Sci 76:119–130CrossRefGoogle Scholar
  52. Ueki I, Stipanuk MH (2008) 3T3-L1 adipocytes and rat adipose tissue have a high capacity for taurine synthesis by the cysteine dioxygenase/cysteinesulfinate decarboxylase and cysteamine dioxygenase pathways. J Nutr 139:207–214PubMedCrossRefPubMedCentralGoogle Scholar
  53. Velasquez A, Pohlenz C, Barrows FT, Gaylord TG, Gatlin DM (2015) Assessment of taurine bioavailability in pelleted and extruded diets with red drum Sciaenops ocellatus. Aquaculture 449:2–7CrossRefGoogle Scholar
  54. Vélez EJ, Lutfi E, Jiménez-Amilburu V, Riera-Codina M, Capilla E, Navarro I, Gutiérrez J (2014) IGF-I and amino acids effects through TOR signaling on proliferation and differentiation of gilthead sea bream cultured myocytes. Gen Comp Endocrinol 205:296–304PubMedCrossRefPubMedCentralGoogle Scholar
  55. Wacyk J, Powell M, Rodnick K, Overturf K, Hill RA, Hardy R (2012) Dietary protein source significantly alters growth performance, plasma variables and hepatic gene expression in rainbow trout (Oncorhynchus mykiss) fed amino acid balanced diets. Aquaculture 356-357:223–234CrossRefGoogle Scholar
  56. Wade NM, Skiba-Cassy S, Dias K, Glencross BD (2014) Postprandial molecular responses in the liver of the barramundi, Lates calcarifer. Fish Physiol Biochem 40:427–443PubMedCrossRefPubMedCentralGoogle Scholar
  57. Wang S-T, Chen H-W, Sheen L-Y, Lii C-K (1997) Methionine and cysteine affect glutathione level, glutathione-related enzyme activities and the expression of glutathione S-transferase isozymes in rat hepatocytes. J Nutr 127:2135–2141PubMedCrossRefPubMedCentralGoogle Scholar
  58. Wang X, He G, Mai K, Xu W, Zhou H (2016) Differential regulation of taurine biosynthesis in rainbow trout and Japanese flounder. Sci Rep 6:1–13CrossRefGoogle Scholar
  59. Wang X, He G, Mai K, Xu W, Zhou H (2017) Molecular cloning and characterization of taurine transporter from turbot (Psetta maxima) and its expression analysis regulated by taurine in vitro. Aquac Res 28:1724–1734CrossRefGoogle Scholar
  60. Watson AM, Barrows FT, Allen R (2015) The importance of taurine and n-3 fatty acids in cobia, Rachycentron canadum. Bull Fish Res Agen 40:51–59Google Scholar
  61. Yokoyama M, Takeuchi T, Park G, Nakazoe J (2001) Hepatic cysteinesulphinate decarboxylase activity in fish. Aquac Res 32:216–220CrossRefGoogle Scholar
  62. Yun B, Ai Q, Mai K, Xu W, Qi G, Luo Y (2012) Synergistic effects of dietary cholesterol and taurine on growth performance and cholesterol metabolism in juvenile turbot (Scophthalmus maximus L.) fed high plant protein diets. Aquaculture 324:85–91CrossRefGoogle Scholar
  63. Zhang Y, Wei Z, Liu G, Deng K, Yang M, Pan M, Gu Z, Liu D, Zhang W, Mai K (2019) Synergistic effects of dietary carbohydrate and taurine on growth performance, digestive enzyme activities and glucose metabolism in juvenile turbot Scophthalmus maximus L. Aquaculture 499:32–41CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2020

Authors and Affiliations

  1. 1.Centre for Animal Science, Queensland Alliance for Agriculture and Food InnovationThe University of QueenslandSt. LuciaAustralia
  2. 2.CSIRO Agriculture and Food, QLD Biosciences PrecinctSt. LuciaAustralia
  3. 3.Institute of Aquaculture, University of StirlingStirlingUK

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