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

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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.

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References

  • 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 10:309–316

    CAS  Google Scholar 

  • Al-Feky SSA, El-Sayed AFM, Ezzat AA (2016a) Dietary taurine improves reproductive performance of Nile tilapia (Oreochromis niloticus) broodstock. Aquac Nutr 22:392–399

    CAS  Google Scholar 

  • 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 22:457–464

    CAS  Google Scholar 

  • Asha K, Devadasan K (2013) Protective effect of taurine on the mitochondria of albino rats induced with fulminant hepatic failure. Biomed Prev Nutr 3:279–283

    Google Scholar 

  • 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):493–503

    CAS  PubMed  Google Scholar 

  • 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 275:201–208

    CAS  Google Scholar 

  • Clemmons DR, Underwood LE (1991) Nutritional regulation of IGF-I and IGF binding proteins. Annu Rev Nutr 11:393–412

    CAS  PubMed  Google Scholar 

  • 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 528:9–23

    CAS  Google Scholar 

  • 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 511:734231

    Google Scholar 

  • 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 13:170–180

    CAS  PubMed  Google Scholar 

  • El-Sayed AFM (2014) Is dietary taurine supplementation beneficial for farmed fish and shrimp? A comprehensive review. Rev Aquac 6:241–255

    Google Scholar 

  • 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 43:349–360

    CAS  Google Scholar 

  • Gabillard JC, Kamangar BB, Montserrat N (2006) Coordinated regulation of the GH/IGF system genes during refeeding in rainbow trout (Oncorhynchus mykiss). J Endocrinol 191:15–24

    CAS  PubMed  Google Scholar 

  • 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 178–228

    Google Scholar 

  • 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 451:298–309

    CAS  Google Scholar 

  • 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 220:749–767

    Google Scholar 

  • Green M, Sambrook J (2012) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • 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 152:39–46

    PubMed  Google Scholar 

  • 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 36:103–112

    CAS  PubMed  Google Scholar 

  • 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 18:1

    Google Scholar 

  • Huxtable R (1992) Physiological actions of taurine. Physiol Rev 72:101–163

    CAS  PubMed  Google Scholar 

  • 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 37:217–226

  • Kaushik SJ, Seiliez I (2010) Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs. Aquac Res 41:322–332

    CAS  Google Scholar 

  • 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 74:875–881

    CAS  Google Scholar 

  • 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 47:1168–1179

    CAS  Google Scholar 

  • 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 433:223–228

    CAS  Google Scholar 

  • Lahnsteiner F, Caberlotto S (2012) Motility of gilthead seabream Sparus aurata spermatozoa and its relation to temperature, energy metabolism and oxidative stress. Aquaculture 370:76–83

    Google Scholar 

  • 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 39:801–810

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • 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 450:349–355

    CAS  Google Scholar 

  • 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 461:1–8

    CAS  Google Scholar 

  • Marshall OJ (2004) PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 20:2471–2472

    CAS  PubMed  Google Scholar 

  • 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 494:19–25

    CAS  Google Scholar 

  • 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 28:374–385

    Google Scholar 

  • Panserat S, Kaushik SJ (2010) Regulation of gene expression by nutritional factors in fish. Aquac Res 41:751–762

    CAS  Google Scholar 

  • 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 179:22–29

    CAS  PubMed  Google Scholar 

  • 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 384-387:1–5

    CAS  Google Scholar 

  • 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 471:213–222

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 

  • Resuehr D, Spiess A-N (2003) A real-time polymerase chain reaction-based evaluation of cDNA synthesis priming methods. Anal Biochem 322:287–291

    CAS  PubMed  Google Scholar 

  • Ripps H, Shen W (2011) Review: Taurine: a “very essential” amino acid. Mol Vis 18:2673–2686

    Google Scholar 

  • 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 181:33–41

    CAS  Google Scholar 

  • 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 114:1784–1796

    CAS  PubMed  Google Scholar 

  • Salze GP, Davis DA (2015) Taurine: a critical nutrient for future fish feeds. Aquaculture 437:215–229

    CAS  Google Scholar 

  • Salze G, McLean E, Craig SR (2012) Dietary taurine enhances growth and digestive enzyme activities in larval cobia. Aquaculture 362:44–49

    Google Scholar 

  • Satriyo TB, Galaviz MA, Salze G, López LM (2017) Assessment of dietary taurine essentiality on the physiological state of juvenile Totoaba macdonaldi. Aquac Res 48:5677–5689

    CAS  Google Scholar 

  • Schuller-Levis GB, Park E (2003) Taurine: new implications for an old amino acid. FEMS Microbiol Lett 226:195–202

    CAS  PubMed  Google Scholar 

  • 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 280:198–205

    CAS  Google Scholar 

  • 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 76:119–130

    CAS  Google Scholar 

  • 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 139:207–214

    PubMed  Google Scholar 

  • 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 449:2–7

    CAS  Google Scholar 

  • 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 205:296–304

    PubMed  Google Scholar 

  • 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 356-357:223–234

    CAS  Google Scholar 

  • Wade NM, Skiba-Cassy S, Dias K, Glencross BD (2014) Postprandial molecular responses in the liver of the barramundi, Lates calcarifer. Fish Physiol Biochem 40:427–443

    CAS  PubMed  Google Scholar 

  • 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 127:2135–2141

    CAS  PubMed  Google Scholar 

  • Wang X, He G, Mai K, Xu W, Zhou H (2016) Differential regulation of taurine biosynthesis in rainbow trout and Japanese flounder. Sci Rep 6:1–13

    Google Scholar 

  • 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 28:1724–1734

    Google Scholar 

  • Watson AM, Barrows FT, Allen R (2015) The importance of taurine and n-3 fatty acids in cobia, Rachycentron canadum. Bull Fish Res Agen 40:51–59

  • Yokoyama M, Takeuchi T, Park G, Nakazoe J (2001) Hepatic cysteinesulphinate decarboxylase activity in fish. Aquac Res 32:216–220

    CAS  Google Scholar 

  • 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 324:85–91

    Google Scholar 

  • 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 499:32–41

    CAS  Google Scholar 

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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

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.

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  1. Centre for Animal Science, Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St. Lucia, QLD, 4067, Australia

    David A. Poppi & Stephen S. Moore

  2. CSIRO Agriculture and Food, QLD Biosciences Precinct, Building 80, Services Road, St. Lucia, QLD, 4067, Australia

    David A. Poppi & Nicholas M. Wade

  3. Institute of Aquaculture, University of Stirling, Stirling, FK9 4LA, UK

    Brett D. Glencross

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  1. David A. Poppi
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Poppi, D.A., Moore, S.S., Wade, N.M. et al. Adequate supply of dietary taurine stimulates expression of molecular markers of growth and protein turnover in juvenile barramundi (Lates calcarifer). Fish Physiol Biochem 46, 953–969 (2020). https://doi.org/10.1007/s10695-020-00762-3

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