Skip to main content
SpringerLink
Log in

Intracellular taurine deficiency impairs cardiac contractility in rainbow trout (Oncorhynchus mykiss) without affecting aerobic performance

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Taurine is a non-proteinogenic sulfonic acid found in high concentrations inside vertebrate cardiomyocytes and its movement across the sarcolemmal membrane is critical for cell volume regulation. Taurine deficiency is rare in mammals, where it impairs cardiac contractility and leads to congestive heart failure. In fish, cardiac taurine levels vary substantially between species and can decrease by up to 60% in response to environmental change but its contribution to cardiac function is understudied. We addressed this gap in knowledge by generating a taurine-deficient rainbow trout (Oncorhynchus mykiss) model using a feed enriched with 3% β-alanine to inhibit cellular taurine uptake. Cardiac taurine was reduced by 17% after 4 weeks with no effect on growth or condition factor. Taurine deficiency did not affect routine or maximum rates of O2 consumption, aerobic scope, or critical swimming speed in whole animals but cardiac contractility was significantly impaired. In isometrically contracting ventricular strip preparations, the force–frequency and extracellular Ca2+-sensitivity relationships were both shifted downward and maximum pacing frequency was significantly lower in β-alanine fed trout. Cardiac taurine deficiency reduces sarcoplasmic reticular Ca2+-ATPase activity in mammals and our results are consistent with such an effect in rainbow trout. Our data indicate that intracellular taurine contributes to the regulation of cardiac contractility in rainbow trout. Aerobic performance was unaffected in β-alanine-fed animals, but further study is needed to determine if more significant natural reductions in taurine may constrain performance under certain environmental conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

Data will be made available upon request.

References

  • Allo SN, Bagby L, Schaffer SW (1997) Taurine depletion, a novel mechanism for cardioprotection from regional ischemia. Am J Physiol 273:H1956–H1961

    CAS  PubMed  Google Scholar 

  • Avella M, Ducoudret O, Pisani DF, Poujeol P (2009) Swelling-activated transport of taurine in cultured gill cells of sea bass: physiological adaptation and pavement cell plasticity. Am J Physiol 296:R1149–R1160. https://doi.org/10.1152/ajpregu.90615.2008

    Article  CAS  Google Scholar 

  • Ballatori N, Simmons TW, Boyer JL (1994) A volume-activated taurine channel in skate hepatocytes: membrane polarity and role of intracellular ATP. Am J Physiol 267:G285–G291. https://doi.org/10.1152/ajpgi.1994.267.2.G285

    Article  CAS  PubMed  Google Scholar 

  • Bers D (2001) Excitation–contraction coupling and cardiac contractile force. Springer Science & Business Media, Berlin

    Google Scholar 

  • Boyd TA, Cha C-J, Forster RP, Goldstein L (1977) Free amino acids in tissues of the skate Raja erinacea and the stingray Dasyatis sabina: Effects of environmental dilution. J Exp Zool 199:435–442

    CAS  PubMed  Google Scholar 

  • Brett JR (1964) The respiratory metabolism and swimming performance of young sockeye salmon. J Fish Res Board Can 21:1183–1226

    Google Scholar 

  • Brittsan AG, Kranias EG (2000) Phospholamban and cardiac contractile function. J Mol Cell Cardiol 12:2131–2139

    Google Scholar 

  • Brosnan JT, Brosnan ME (2006) The sulfur-containing amino acids: an overview. J Nutr 136:1636S-1640S

    CAS  PubMed  Google Scholar 

  • Callaghan NI, Williams KJ, Bennett JC, MacCormack TJ (2017) Nanoparticulate-specific effects of silver on teleost cardiac contractility. Environ Pollut 237:721–730

    PubMed  Google Scholar 

  • Claireaux G, McKenzie DJ, Genge AG, Chatelier A, Aubin J, Farrell AP (2005) Linking swimming performance, cardiac pumping ability and cardiac anatomy in rainbow trout. J Exp Biol 208:1775–1784. https://doi.org/10.1242/jeb.01587

    Article  PubMed  Google Scholar 

  • Clow KA, Rodnick KJ, MacCormack TJ, Driedzic WR (2004) The regulation and importance of glucose uptake in the isolated Atlantic cod heart: rate-limiting steps and effects of hypoxia. J Exp Biol 207:1865–1874

    CAS  PubMed  Google Scholar 

  • Dawson RJ, Biasetti M, Messina S, Dominy J (2002) The cytoprotective role of taurine in exercise-induced muscle injury. Amino Acids 22:309–324

    CAS  PubMed  Google Scholar 

  • De La Puerta C (2010) Taurine and glucose metabolism: a review. Nutr Hosp 25:910–919. https://doi.org/10.3305/nh.2010.25.6.4815

    Article  CAS  PubMed  Google Scholar 

  • Eley DW, Lake N, Ter HK (1994) Taurine depletion and excitation-contraction coupling in rat myocardium. Circ Res 74:1210–1219

    CAS  PubMed  Google Scholar 

  • Eliason EJ, Farrell AP (2016) Oxygen uptake in Pacific salmon Oncorhynchus spp.: when ecology and physiology meet. J Fish Biol 88:359–388. https://doi.org/10.1111/jfb.12790

    Article  CAS  PubMed  Google Scholar 

  • Farrell AP (2009) Environment, antecedents and climate change: lessons from the study of temperature physiology and river migration of salmonids. J Exp Biol 212:3771–3780. https://doi.org/10.1242/jeb.023671

    Article  CAS  PubMed  Google Scholar 

  • Farrell AP, Johansen JA, Suarez RK (1991) Effects of exercise-training on cardiac performance and muscle enzymes in rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 9:303–312

    CAS  PubMed  Google Scholar 

  • Franconi F, Martini F, Stendardi I, Matucci R, Zilletti L, Giotti A (1982) Effect of taurine on calcium levels and contractility in guinea-pig ventricular strips. Biochem Pharmacol 31:3181–3185. https://doi.org/10.1016/0006-2952(82)90547-0

    Article  CAS  PubMed  Google Scholar 

  • Fugelli K, Vislie T (1982) Physiological response to acid water in brown trout (Salmo trutta L.): cell volume regulation in heart ventricle tissue. J Exp Biol 101:71–82

    CAS  PubMed  Google Scholar 

  • Fujita KK, Xia Z, Tomy G, Montina T, Wiseman S (2021) 1H NMR based metabolomic profiling of early life stage zebrafish (Danio rerio) exposed to a water-soluble fraction of weathered sediment-bound diluted bitumen. Aquat Toxicol 232:105766. https://doi.org/10.1016/j.aquatox.2021.105766

    Article  CAS  PubMed  Google Scholar 

  • Galler S, Hutzler C, Haller T (1990) Effects of taurine on Ca2+-dependent force development of skinned muscle fibre preparations. J Exp Biol 152:255–264

    CAS  PubMed  Google Scholar 

  • Goldstein L, Luer CA, Blum PC (1990) Taurine accumulation by the heart of embryonic skates, Raja eglanteria. J Exp Biol 150:449–452

    CAS  PubMed  Google Scholar 

  • Goto T, Tiba K, Sakurada Y, Takagi S (2001) Determination of hepatic cysteinesulfinate decarboxylase activity in fish by means of OPA-prelabeling and reverse-phase high-performance liquid chromatographic separation. Fish Sci 67:553–555

    CAS  Google Scholar 

  • Goto T, Matsumoto T, Murakami S, Takagi S, Hasumi F (2003) Conversion of cysteate into taurine in liver of fish. Fish Sci 69:216–218

    CAS  Google Scholar 

  • Gras J, Gudefin Y, Chagny F, Perrier H (1982) Free amino acids and ninhydrin-positive substances in fish—II. Cardio-respiratory system: Plasma, erythrocytes, heart and gills of the rainbow trout (Salmo gairdnerii Richardson). Comp Biochem Physiol Part B Comp Biochem 73:845–847. https://doi.org/10.1016/0305-0491(82)90327-3

    Article  CAS  Google Scholar 

  • Henry EF, MacCormack TJ (2018) Taurine protects cardiac contractility in killifish, Fundulus heteroclitus, by enhancing sarcoplasmic reticular Ca2+ cycling. J Comp Physiol B 188:89–99

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ito T, Oishi S, Takai M, Kimura Y, Uozumi Y, Fujio Y, Schaffer SW, Azuma J (2010) Cardiac and skeletal muscle abnormality in taurine transporter-knockout mice. J Biomed Sci 17:S20

    PubMed  PubMed Central  Google Scholar 

  • Jain KE, Hamilton JC, Farrell AP (1997) Use of a ramp velocity test to measure critical swimming speed in rainbow trout (Onchorhynchus mykiss). Comp Biochem Physiol A Physiol 117:441–444

    Google Scholar 

  • Kaplan JL, Stern JA, Fascetti AJ, Larsen JA, Skolnik H, Peddle GD, Kienle RD, Waxman A, Cocchiaro M, Gunther-Harrington CT, Klose T, LaFauci K, Lefbom B, Machen Lamy M, Malakoff R, Nishimura S, Oldach M, Rosenthal S, Stauthammer C, O’Sullivan L, Visser LC, William R, Ontiveros E (2018) Taurine deficiency and dilated cardiomyopathy in golden retrievers fed commercial diets. PLoS ONE 13:e0209112. https://doi.org/10.1371/journal.pone.0209112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim SK, Takeuchi T, Yokoyama M, Murata Y, Kaneniwa M, Sakakura Y (2005) Effect of dietary taurine levels on growth and feeding behavior of juvenile Japanese flounder Paralichthys olivaceus. Aquaculture 250:765–774

    CAS  Google Scholar 

  • Kim S-K, Matsunari H, Takeuchi T, Yokoyama M, Furuita H, Murata Y, Goto T (2008) Comparison of taurine biosynthesis ability between juveniles of Japanese flounder and common carp. Amino Acids 35:161–168

    CAS  PubMed  Google Scholar 

  • King PA, Cha C-J, Goldstein L (1980) Amino acid metabolism and cell volume regulation in the little skate, Raja erinacea. I Oxidation J Exp Zool 212:69–77

    CAS  Google Scholar 

  • Layland J, Young IS, Altringham JD (1995) The effect of cycle frequency on the power output of rat papillary muscles in vitro. J Exp Biol 198:1035–1043

    CAS  PubMed  Google Scholar 

  • Lyndon AR, Davidson I, Houlihan DF (1993) Changes in tissue and plasma free amino acid concentrations after feeding in Atlantic cod. Fish Physiol Biochem 10:365–375. https://doi.org/10.1007/BF00004503

    Article  CAS  PubMed  Google Scholar 

  • MacCormack TJ, Driedzic WR (2002) Mitochondrial ATP-sensitive K+ channels influence force development and anoxic contractility in a flatfish, yellowtail flounder Limanda ferruginea, but not Atlantic cod Gadus morhua heart. J Exp Biol 205:1411–1418

    CAS  PubMed  Google Scholar 

  • MacCormack TJ, Callaghan NI, Sykes AV, Driedzic WR (2016) Taurine depresses cardiac contractility and enhances systemic heart glucose utilization in the cuttlefish, Sepia officinalis. J Comp Physiol B 186:215–227

    CAS  PubMed  Google Scholar 

  • MacNutt MJ, Hinch SG, Farrell AP, Topp S (2004) The effect of temperature and acclimation period on repeat swimming performance in cutthroat trout. J Fish Biol 65:342–353. https://doi.org/10.1111/j.0022-1112.2004.00453.x

    Article  Google Scholar 

  • Mezzomo NJ, Silveira A, Giuliani GS, Quadros VA, Rosemberg DB (2016) The role of taurine on anxiety-like behaviors in zebrafish: a comparative study using the novel tank and the light–dark tasks. Neurosci Lett 613:19–24. https://doi.org/10.1016/j.neulet.2015.12.037

    Article  CAS  PubMed  Google Scholar 

  • Mezzomo NJ, Fontana BD, Müller TE, Duarte T, Quadros VA, Canzian J, Pompermaier A, Soares SM, Koakoski G, Loro VL, Rosemberg DB, Barcellos LJG (2019) Taurine modulates the stress response in zebrafish. Horm Behav 109:44–52. https://doi.org/10.1016/j.yhbeh.2019.02.006

    Article  CAS  PubMed  Google Scholar 

  • Miles AR, Hawrysh PJ, Hossein-Javaheri N, Buck LT (2018) Taurine activates glycine and GABAA receptor currents in anoxia-tolerant painted turtle pyramidal neurons. J Exp Biol 221:181529. https://doi.org/10.1242/jeb.181529

    Article  Google Scholar 

  • Pansani MC, Azevedo PS, Rafacho BPM, Minicucci MF, Chiuso-Minicucci F, Zorzella-Pezavento SG, Marchini JS, Padovan GJ, Fernandes AAH, Matsubara BB, Matsubara LS, Zornoff LAM, Paiva SAR (2012) atrophic cardiac remodeling induced by taurine deficiency in Wistar rats. PLoS ONE 7:41439

    Google Scholar 

  • Peake SJ, Farrell AP (2006) What triggers fatigue in respirometer-confined fishes. J Fish Biol 68:1742–1755

    Google Scholar 

  • Pinto W, Rønnestad I, Jordal A-EO, Gomes AS, Dinis MT, Aragão C (2012) Cloning, tissue and ontogenetic expression of the taurine transporter in the flatfish Senegalese sole (Solea senegalensis). Amino Acids 42:1317–1327

    CAS  PubMed  Google Scholar 

  • Postlethwaite EK, Mcdonald DG (1995) Mechanisms of Na+ and Cl− regulation in freshwater-adapted rainbow trout (Oncorhychus mykiss) during exercise and stress. J Exp Biol 198:295–304

    CAS  PubMed  Google Scholar 

  • Ramila KC, Jong CJ, Pastukh V, Ito T, Azuma J, Schaffer SW (2015) Role of protein phosphorylation in excitation-contraction coupling in taurine deficient hearts. Am J Physiol 308:H232–H239. https://doi.org/10.1152/ajpheart.00497.2014

    Article  CAS  Google Scholar 

  • Ravens U, Link S, Gath J, Noble MIM (1995) Post-rest potentiation and its decay after inotropic interventions in isolated rat heart muscle. Pharmacol Toxicol 76:9–16

    CAS  PubMed  Google Scholar 

  • Sakaguchi M, Murata M, Kawai A (1982) Taurine levels in some tissues of yellowtail (Seriola quinqueradiata) and mackerel (Scomber japonicus). Agric Biol Chem 46:2857–2858

    CAS  Google Scholar 

  • Salze GP, Davis DA (2015) Taurine: a critical nutrient for future fish feeds. Aquaculture 437:215–229. https://doi.org/10.1016/j.aquaculture.2014.12.006

    Article  CAS  Google Scholar 

  • Sardella BA, Brauner CJ (2007) The osmo-respiratory compromise in fish. In: Fernandes MN (ed) Fish respiration and environment. Science Publishers, Enfield, pp 147–165

    Google Scholar 

  • Schaffer SW, Ballard C, Azuma J (1994) Mechanisms underlying physiological and pharmacological actions of taurine on myocardial calcium transport. Taurine in health and disease. Advances in experimental medicine and biology. Springer, Boston, pp 171–180

    Google Scholar 

  • Schaffer SW, Ju Jong C, Ramila KC, Azuma J (2010) Physiological roles of taurine in heart and muscle. J Biomed Sci 17:S2

    PubMed  PubMed Central  Google Scholar 

  • Schaffer SW, Jong CJ, Ito T, Azuma J (2014) Effect of taurine on ischemia–reperfusion injury. Amino Acids 46:21–30. https://doi.org/10.1007/s00726-012-1378-8

    Article  CAS  PubMed  Google Scholar 

  • Shiels HA, Farrell AP (1997) The effect of temperature and adrenaline on the relative importance of the sarcoplasmic reticulum in contributing Ca2+ to force development in isolated ventricular trabeculae from rainbow trout. J Exp Biol 200:1606–1621

    Google Scholar 

  • Shiels HA, Galli GLJ (2014) The sarcoplasmic reticulum and the evolution of the vertebrate heart. Physiology 29:456–469

    CAS  PubMed  Google Scholar 

  • Shiels HA, Sitsapesan R (2015) Is there something fishy about the regulation of the ryanodine receptor in the fish heart? Fish cardiac ryanodine receptor 2 regulation. Exp Physiol 100:1412–1420. https://doi.org/10.1113/EP085136

    Article  CAS  PubMed  Google Scholar 

  • Shiels HA, Vornanen M, Farrell AP (2002) The force–frequency relationship in fish hearts—a review. Comp Biochem Physiol A 132:811–826. https://doi.org/10.1016/S1095-6433(02)00050-8

    Article  Google Scholar 

  • Shiels HA, Santiago DA, Galli GLJ (2010) Hypercapnic acidosis reduces contractile function in the ventricle of the armored catfish, Pterygoplichthys Pardalis. Physiol Biochem Zool PBZ 83:366–375

    CAS  PubMed  Google Scholar 

  • Steele DS, Smith GL, Miller DJ (1990) The effects of taurine on Ca2+ uptake by the sarcoplasmic reticulum and Ca2+ sensitivity of chemically skinned rat heart. J Physiol 422:499–511. https://doi.org/10.1113/jphysiol.1990.sp017997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takeuchi K, Toyohara H, Sakaguchi M (2000) A hyperosmotic stress-induced mRNA of carp cell encodes Na- and Cl3-dependent high affinity taurine transporter. Biochim Biophys Acta 1464:219–230

    CAS  PubMed  Google Scholar 

  • Takeuchi K, Toyohara H, Kinoshita M, Sakaguchi M (2001) Ubiquitous increase in taurine transporter mRNA in tissues of tilapia (Oreochromis mossambicus) during high-salinity adaptation. Fish Physiol Biochem 23:173–182

    Google Scholar 

  • Vislie T (1980) Hyper-osmotic cell volume regulation in vivo and in vitro in flounder (Platichthys flesus) heart ventricles. J Comp Physiol B 140:185–191. https://doi.org/10.1007/BF00690402

    Article  Google Scholar 

  • Vislie T (1983) Cell volume regulation in fish heart ventricles with special reference to taurine. Comp Biochem Physiol A 76:507–514

    CAS  PubMed  Google Scholar 

  • Vislie T, Fugelli K (1975) Cell volume regulation in flounder (Platichthys flesus) heart muscle accompanying an alteration in plasma osmolality. Comp Biochem Physiol A Physiol 52:415–418. https://doi.org/10.1016/S0300-9629(75)80057-0

    Article  CAS  Google Scholar 

  • Wood CM, Randall DJ (1973) The influence of swimming activity on water balance in the rainbow trout (Salmo gairdneri). J Comp Physiol 82:257–276. https://doi.org/10.1007/BF00694239

    Article  Google Scholar 

  • Wood CM, Walsh PJ, Kajimura M, McClelland GB, Chew SF (2010) The influence of feeding and fasting on plasma metabolites in the dogfish shark (Squalus acanthias). Comp Biochem Physiol A 155:435–444. https://doi.org/10.1016/j.cbpa.2009.09.006

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Zarate JM, Bradley TM (2007) Molecular cloning and characterization of the taurine transporter of Atlantic salmon. Aquaculture 273:209–217. https://doi.org/10.1016/j.aquaculture.2007.10.002

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Jim Duston, Ms. Audrie-Jo McConkey, Ms. Jamie Fraser, and Mr. Kare Tonning for considerable technical assistance with the preparation of the experimental feed and completion of the initial feeding trial. We also thank Mr. Wayne Anderson for animal husbandry assistance.

Funding

MAG was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) undergraduate student research assistantship. AJM, SGL, and TJM were supported by NSERC Discovery Grants.

Author information

Authors and Affiliations

  1. Department of Chemistry and Biochemistry, Mount Allison University, 63C York St., Sackville, NB, E4L1G8, Canada

    M. A. Gates, A. J. Morash, S. G. Lamarre & T. J. MacCormack

  2. Department of Biology, Mount Allison University, Sackville, NB, Canada

    M. A. Gates, A. J. Morash, S. G. Lamarre & T. J. MacCormack

  3. Department of Biology, Université de Moncton, Moncton, NB, Canada

    M. A. Gates, A. J. Morash, S. G. Lamarre & T. J. MacCormack

Authors
  1. M. A. Gates
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. J. Morash
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. G. Lamarre
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. J. MacCormack
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the design of the study, carrying out experiments, analyzing data, and the preparation of the manuscript.

Corresponding author

Correspondence to T. J. MacCormack.

Ethics declarations

Conflicts of interest

The authors declare no conflicts of interest.

Additional information

Communicated by B. Pelster.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gates, M.A., Morash, A.J., Lamarre, S.G. et al. Intracellular taurine deficiency impairs cardiac contractility in rainbow trout (Oncorhynchus mykiss) without affecting aerobic performance. J Comp Physiol B 192, 49–60 (2022). https://doi.org/10.1007/s00360-021-01407-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-021-01407-4

Keywords

Search

Navigation