Skip to main content
Log in

Mechanism of osmoregulatory adaptation in tilapia

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

The shortage of freshwater resource in many countries leads to a shift to develop aquaculture in brackish water and sea water. Tilapias are euryhaline that can thrive from freshwater to full sea water. They and their hybrids are the best candidate species for cultivation in brackish habitats. Thus, understanding their osmoregulatory mechanisms will help to breed or genetically engineer salt tolerant species. In this paper, we review recent progress in understanding the mechanisms of osmoregulatory adaptations in tilapia.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Kamal AHMM, Mair GC (2005) Salinity tolerance in superior genotypes of tilapia, Oreochromis niloticus, Oreochromis mossambicus and their hybrids. Aquaculture 247:189–201

    Article  Google Scholar 

  2. Thodesen J, Rye M, Wang YX, Yang KS, Bentsen HB et al (2011) Genetic improvement of tilapias in China: genetic parameters and selection responses in growth of Nile tilapia (Oreochromis niloticus) after six generations of multi-trait selection for growth and fillet yield. Aquaculture 322–323:51–64

    Article  Google Scholar 

  3. Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283

    Article  PubMed  CAS  Google Scholar 

  4. Yan B, Wang Z (2010) Growth, salinity tolerance and microsatellite analysis of the F2 reciprocal hybrids of Oreochromis niloticus × Sarotherodon galilaeus at different salinities. Aquac Res 41:e336–e344

    Article  CAS  Google Scholar 

  5. Wang PJ, Lin CH, Hwang LY, Huang CL, Lee TH et al (2009) Differential responses in gills of euryhaline tilapia, Oreochromis mossambicus, to various hyperosmotic shocks. Comp Biochem Physiol 152:544–551

    Article  Google Scholar 

  6. Lutz CG, Armas-Rosales AM, Saxton AM (2010) Genetic effects influencing salinity tolerance in six varieties of tilapia (Oreochromis) and their reciprocal crosses. Aquac Res 41:e770–e780

    Article  CAS  Google Scholar 

  7. Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177

    Article  PubMed  CAS  Google Scholar 

  8. Gonzalez R (2011) The physiology of hyper-salinity tolerance in teleost fish. J Comp Physiol B 182(3):321–329

    Article  PubMed  Google Scholar 

  9. Smith HW (1930) The absorption and excretion of water and salts by marine teleosts. Am J Physiol 93:480–505

    CAS  Google Scholar 

  10. Grosell M, Laliberte C, Wood S, Jensen FB, Wood C (2001) Intestinal HCO3 secretion in marine teleost fish: evidence for an apical rather than a basolateral Cl/HCO3 exchanger. Fish Physiol Biochem 24:81–95

    Article  CAS  Google Scholar 

  11. Grosell M, Taylor JR (2007) Intestinal anion exchange in teleost water balance. Comp Biochem Physiol A 148:14–22

    Google Scholar 

  12. McCormick SD (2001) Endocrine control of osmoregulation in teleost fish. Am Zool 41:781–794

    Article  CAS  Google Scholar 

  13. Sakamoto T, McCormick SD (2006) Prolactin and growth hormone in fish osmoregulation. Gen Comp Endocrinol 147:24–30

    Article  PubMed  CAS  Google Scholar 

  14. Fiol DF, Kültz D (2007) Osmotic stress sensing and signaling in fishes. FEBS J 274:5790–5798

    Article  PubMed  CAS  Google Scholar 

  15. Hiroi J, McCormick SD, Ohtani-Kaneko R, Kaneko T (2005) Functional classification of mitochondrion-rich cells in euryhaline Mozambique tilapia (Oreochromis mossambicus) embryos, by means of triple immunofluorescence staining for Na+/K+-ATPase, Na+/K+/2Cl cotransporter and CFTR anion channel. J Exp Biol 208:2023–2036

    Article  PubMed  CAS  Google Scholar 

  16. Evans T (2010) Co-ordination of osmotic stress responses through osmosensing and signal transduction events in fishes. J Fish Biol 76:1903–1925

    Article  PubMed  CAS  Google Scholar 

  17. Aruna A, Nagarajan G, Chang CF (2012) Involvement of corticotropin-releasing hormone and corticosteroid receptors in the brain-pituitary-gill of tilapia during the course of seawater acclimation. J Neuroendocrinol 24(5):818–830

    Article  PubMed  CAS  Google Scholar 

  18. Lorin-Nebel C, Avarre JC, Faivre N, Wallon S, Charmantier G et al (2012) Osmoregulatory strategies in natural populations of the black-chinned tilapia Sarotherodon melanotheron exposed to extreme salinities in West African estuaries. J Comp Physiol B 182(6):771–780

    Article  PubMed  CAS  Google Scholar 

  19. Bole-Feysot C, Goffin V, Edery M, Binart N, Kelly PA (1998) Prolactin (PRL) and its receptor: actions, signal transduction pathways, and phenotypes observed in PRL receptor knockout mice. Endocr Rev 19:225–268

    Article  PubMed  CAS  Google Scholar 

  20. Sakamoto T, Fujimoto M, Ando M (2003) Fishy tales of prolactin-releasing peptide. Int Rev Cytol 225:91–130

    Article  PubMed  CAS  Google Scholar 

  21. Harris J, Stanford M, Oakes R, Ormandy J (2004) Prolactin and the prolactin receptor: new targets of an old hormone. Ann Med 36:414–425

    Article  PubMed  CAS  Google Scholar 

  22. Herndon TM, McCormick SD, Bern HA (1991) Effects of prolactin on chloride cells in opercular membrane of seawater-adapted tilapia. Gen Comp Endocrinol 83:283–289

    Article  PubMed  CAS  Google Scholar 

  23. Pisam M, Auperin B, Prunet P, Rentier-Delrue F, Martial J et al (1993) Effects of prolactin on α and β chloride cells in the gill epithelium of the saltwater adapted tilapia “Oreochromis niloticus”. Anat Rec 235:275–284

    Article  PubMed  CAS  Google Scholar 

  24. Breves J, Hasegawa S, Yoshioka M, Fox B, Davis L et al (2010) Acute salinity challenges in Mozambique and Nile tilapia: differential responses of plasma prolactin, growth hormone and branchial expression of ion transporters. Gen Comp Endocrinol 167:135–142

    Article  PubMed  CAS  Google Scholar 

  25. McCormick SD (1995) Hormonal control of gill Na+,K+-ATPase and chloride cell function. Fish Physiol 14:285–315

    Article  CAS  Google Scholar 

  26. Björnsson BT (1997) The biology of salmon growth hormone: from daylight to dominance. Fish Physiol Biochem 17:9–24

    Article  Google Scholar 

  27. Sakamoto T, McCormick SD, Hirano T (1993) Osmoregulatory actions of growth hormone and its mode of action in salmonids. Fish Physiol Biochem 11:155–164

    Article  CAS  Google Scholar 

  28. Mancera J, McCormick S (1999) Influence of cortisol, growth hormone, insulin-like growth factor I and 3,3′,5-triiodo-l-thyronine on hypoosmoregulatory ability in the euryhaline teleost Fundulus heteroclitus. Fish Physiol Biochem 21:25–33

    Article  CAS  Google Scholar 

  29. Pelis RM, McCormick SD (2001) Effects of growth hormone and cortisol on Na+-K+-2Cl-cotransporter localization and abundance in the gills of Atlantic salmon. Gen Comp Endocrinol 124:134–143

    Article  PubMed  CAS  Google Scholar 

  30. Kammerer BD, Cech JJ Jr, Kültz D (2010) Rapid changes in plasma cortisol, osmolality, and respiration in response to salinity stress in tilapia (Oreochromis mossambicus). Comp Biochem Physiol A 157:260–265

    Article  Google Scholar 

  31. Kiilerich P, Tipsmark CK, Borski RJ, Madsen SS (2011) Differential effects of cortisol and 11-deoxycorticosterone on ion transport protein mRNA levels in gills of two euryhaline teleosts, Mozambique tilapia (Oreochromis mossambicus) and striped bass (Morone saxatilis). J Endocrinol 209:115–126

    Article  PubMed  CAS  Google Scholar 

  32. Perry SF (1997) The chloride cell: structure and function in the gills of freshwater fishes. Annu Rev Physiol 59:325–347

    Article  PubMed  CAS  Google Scholar 

  33. Marshall W, Bryson S (1998) Transport mechanisms of seawater teleost chloride cells: an inclusive model of a multifunctional cell. Comp Biochem Physiol A 119:97–106

    Article  CAS  Google Scholar 

  34. Heijden A, Verbost P, Eygensteyn J, Li J, Bonga S et al (1997) Mitochondria-rich cells in gills of tilapia (Oreochromis mossambicus) adapted to fresh water or sea water: quantification by confocal laser scanning microscopy. J Exp Biol 200:55–64

    PubMed  Google Scholar 

  35. Lee TH, Feng SH, Lin CH, Hwang YH, Huang CL et al (2003) Ambient salinity modulates the expression of sodium pumps in branchial mitochondria-rich cells of Mozambique tilapia, Oreochromis mossambicus. Zool Sci 20:29–36

    Article  PubMed  CAS  Google Scholar 

  36. Choi JH, Lee KM, Inokuchi M, Kaneko T (2011) Morphofunctional modifications in gill mitochondria-rich cells of Mozambique tilapia transferred from freshwater to 70 % seawater, detected by dual observations of whole-mount immunocytochemistry and scanning electron microscopy. Comp Biochem Physiol A 158:132–142

    Google Scholar 

  37. Kammerer B, Sardella B, Kültz D (2009) Salinity stress results in rapid changes in cell cycle of tilapia (Oreochromis mossambicus) gill epithelial cells. J Exp Zool 311A:80–90

    Article  Google Scholar 

  38. Ouattara NG, Bodinier C, Nègre-Sadargues G, D’Cotta H, Messad S et al (2009) Changes in gill ionocyte morphology and function following transfer from fresh to hypersaline waters in the tilapia Sarotherodon melanotheron. Aquaculture 290:155–164

    Article  CAS  Google Scholar 

  39. Sardella BA, Matey V, Cooper J, Gonzalez RJ, Brauner CJ (2004) Physiological, biochemical and morphological indicators of osmoregulatory stress in ‘California’Mozambique tilapia (Oreochromis mossambicus × O. urolepis hornorum) exposed to hypersaline water. J Exp Biol 207:1399–1413

    Article  PubMed  CAS  Google Scholar 

  40. Hwang PP, Lee TH (2007) New insights into fish ion regulation and mitochondrion-rich cells. Comp Biochem Physiol A 148:479–497

    Article  Google Scholar 

  41. Tang CH, Chang IC, Chen CH, Lee TH, Hwang PP (2008) Phenotypic changes in mitochondrion-rich cells and responses of Na+/K+-ATPase in gills of tilapia exposed to deionized water. Zool Sci 25:205–211

    Article  PubMed  CAS  Google Scholar 

  42. Scheiner-Bobis G (2002) The sodium pump. Eur J Biochem 269:2424–2433

    Article  PubMed  CAS  Google Scholar 

  43. Xie Z, Askari A (2002) Na+/K+-ATPase as a signal transducer. Eur J Biochem 269:2434–2439

    Article  PubMed  CAS  Google Scholar 

  44. Lin LY, Hwang PP (2001) Modification of morphology and function of integument mitochondria-rich cells in tilapia larvae (Oreochromis mossambicus) acclimated to ambient chloride levels. Physiol Biochem Zool 74:469–476

    Article  PubMed  CAS  Google Scholar 

  45. Lytle C, Xu JC, Biemesderfer D, Forbush B (1995) Distribution and diversity of Na–K–Cl cotransport proteins: a study with monoclonal antibodies. Am J Physiol 269:C1496–C1505

    PubMed  CAS  Google Scholar 

  46. Gamba G, Miyanoshita A, Lombardi M, Lytton J, Lee WS et al (1994) Molecular cloning, primary structure, and characterization of two members of the mammalian electroneutral sodium-(potassium)-chloride cotransporter family expressed in kidney. J Biol Chem 269:17713–17722

    PubMed  CAS  Google Scholar 

  47. Payne JA, Forbush B (1995) Molecular characterization of the epithelial Na–K–Cl cotransporter isoforms. Curr Opin Cell Biol 7:493–503

    Article  PubMed  CAS  Google Scholar 

  48. Hiroi J, Yasumasu S, McCormick SD, Hwang PP, Kaneko T (2008) Evidence for an apical Na–Cl cotransporter involved in ion uptake in a teleost fish. J Exp Biol 211:2584–2599

    Article  PubMed  CAS  Google Scholar 

  49. Horng JL, Lin LY (2008) Expression of the Na–K–2Cl cotransporter in branchial mitochondrion-Rich cells of Mozambique tilapia (Oreochromis mossambicus) subjected to varying chloride conditions. Zool Stud 47:733–740

    CAS  Google Scholar 

  50. Tse WKF, Au DWT, Wong CKC (2006) Characterization of ion channel and transporter mRNA expressions in isolated gill chloride and pavement cells of seawater acclimating eels. Biochem Biophys Res Commun 346:1181–1190

    Article  PubMed  CAS  Google Scholar 

  51. Sardella BA, Kültz D (2009) Osmo-and ionoregulatory responses of green sturgeon (Acipenser medirostris) to salinity acclimation. J Comp Physiol B 179:383–390

    Article  PubMed  Google Scholar 

  52. Bodinier C, Boulo V, Lorin-Nebel C, Charmantier G (2009) Influence of salinity on the localization and expression of the CFTR chloride channel in the ionocytes of Dicentrarchus labrax during ontogeny. J Anat 214:318–329

    Article  PubMed  CAS  Google Scholar 

  53. Marshall WS (2002) Na+, Cl, Ca2+ and Zn2+ transport by fish gills: retrospective review and prospective synthesis. J Exp Zool 293:264–283

    Article  PubMed  CAS  Google Scholar 

  54. Shaw JR, Sato D, VanderHeide J, LaCasse T, Stanton CR et al (2008) The role of SGK and CFTR in acute adaptation to seawater in Fundulus heteroclitus. Cell Physiol Biochem 22:069–078

    Article  CAS  Google Scholar 

  55. Scott GR, Richards JG, Forbush B, Isenring P, Schulte PM (2004) Changes in gene expression in gills of the euryhaline killifish Fundulus heteroclitus after abrupt salinity transfer. Am J Physiol 287:C300–C309

    Article  CAS  Google Scholar 

  56. Daborn K, Cozzi R, Marshall W (2001) Dynamics of pavement cell–chloride cell interactions during abrupt salinity change in Fundulus heteroclitus. J Exp Biol 204:1889–1899

    PubMed  CAS  Google Scholar 

  57. Lin LY, Hwang PP (2004) Mitochondria-rich cell activity in the yolk-sac membrane of tilapia (Oreochromis mossambicus) larvae acclimatized to different ambient chloride levels. J Exp Biol 207:1335–1344

    Article  PubMed  CAS  Google Scholar 

  58. Miyazaki H, Kaneko T, Uchida S, Sasaki S, Takei Y (2002) Kidney-specific chloride channel, OmClC-K, predominantly expressed in the diluting segment of freshwater-adapted tilapia kidney. Proc Natl Acad Sci USA 99:15782–15787

    Article  PubMed  CAS  Google Scholar 

  59. Loretz CA, Pollina C, Hyodo S, Takei Y, Chang W et al (2004) cDNA cloning and functional expression of a Ca2+-sensing receptor with truncated C-terminal tail from the Mozambique tilapia (Oreochromis mossambicus). J Biol Chem 279:53288–53297

    Article  PubMed  CAS  Google Scholar 

  60. Loretz CA, Pollina C, Hyodo S, Takei Y (2009) Extracellular calcium-sensing receptor distribution in osmoregulatory and endocrine tissues of the tilapia. Gen Comp Endocrinol 161:216–228

    Article  PubMed  CAS  Google Scholar 

  61. Cutler CP, Martinez AS, Cramb G (2007) The role of aquaporin 3 in teleost fish. Comp Biochem Physiol A 148:82–91

    Article  Google Scholar 

  62. Watanabe S, Hirano T, Grau EG, Kaneko T (2009) Osmosensitivity of prolactin cells is enhanced by the water channel aquaporin-3 in a euryhaline Mozambique tilapia (Oreochromis mossambicus). Am J Physiol 296:R446–R453

    CAS  Google Scholar 

  63. Watanabe S, Kaneko T, Aida K (2005) Aquaporin-3 expressed in the basolateral membrane of gill chloride cells in Mozambique tilapia Oreochromis mossambicus adapted to freshwater and seawater. J Exp Biol 208:2673–2682

    Article  PubMed  CAS  Google Scholar 

  64. Haas M, Forbush B III (2000) The Na–K–Cl cotransporter of secretory epithelia. Annu Rev Physiol 62:515–534

    Article  PubMed  CAS  Google Scholar 

  65. Inokuchi M, Hiroi J, Watanabe S, Lee KM, Kaneko T (2008) Gene expression and morphological localization of NHE3, NCC and NKCC1a in branchial mitochondria-rich cells of Mozambique tilapia (Oreochromis mossambicus) acclimated to a wide range of salinities. Comp Biochem Physiol A 151:151–158

    Article  Google Scholar 

  66. Breves JP, Seale AP, Helms RE, Tipsmark CK, Hirano T et al (2011) Dynamic gene expression of GH/PRL-family hormone receptors in gill and kidney during freshwater-acclimation of Mozambique tilapia. Comp Biochem Physiol A 158:194–200

    Article  Google Scholar 

  67. Pierce A, Fox B, Davis L, Visitacion N, Kitahashi T et al (2007) Prolactin receptor, growth hormone receptor, and putative somatolactin receptor in Mozambique tilapia: tissue specific expression and differential regulation by salinity and fasting. Gen Comp Endocrinol 154:31–40

    Article  PubMed  CAS  Google Scholar 

  68. Sandra O, Le Rouzic P, Rentier-Delrue F, Prunet P (2001) Transfer of tilapia (Oreochromis niloticus) to a hyperosmotic environment is associated with sustained expression of prolactin receptor in intestine, gill, and kidney. Gen Comp Endocrinol 123:295–307

    Article  PubMed  CAS  Google Scholar 

  69. Shiraishi K, Matsuda M, Mori T, Hirano T (1999) Changes in expression of prolactin-and cortisol-receptor genes during early-life stages of euryhaline tilapia (Oreochromis mossambicus) in fresh water and seawater. Zool Sci 16:139–146

    Article  CAS  Google Scholar 

  70. Magdeldin S, Uchida K, Hirano T, GRAU EG, Abdelfattah A et al (2007) Effects of environmental salinity on somatic growth and growth hormone/insulin-like growth factor-I axis in juvenile tilapia Oreochromis mossambicus. Fish Sci 73:1025–1034

    Article  CAS  Google Scholar 

  71. Varsamos S, Nebel C, Charmantier G (2005) Ontogeny of osmoregulation in postembryonic fish. Comp Biochem Physiol A 141:401–429

    Article  Google Scholar 

  72. Fiol DF, Kültz D (2005) Rapid hyperosmotic coinduction of two tilapia (Oreochromis mossambicus) transcription factors in gill cells. Proc Natl Acad Sci USA 102:927–932

    Article  PubMed  CAS  Google Scholar 

  73. Winter J, Jung S, Keller S, Gregory RI, Diederichs S (2009) Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11:228–234

    Article  PubMed  CAS  Google Scholar 

  74. Flynt AS, Thatcher EJ, Burkewitz K, Li N, Liu Y et al (2009) miR-8 microRNAs regulate the response to osmotic stress in zebrafish embryos. J Cell Biol 185:115–127

    Article  PubMed  CAS  Google Scholar 

  75. Yan B, Guo JT, Zhao LH, Zhao JL (2012) MiR-30c: a novel regulator of salt tolerance in tilapia. Biochem Biophys Res Commun 425(2):315–320

    Google Scholar 

  76. Yan B, Zhao LH, Guo JT, Zhao JL (2012) miR-429 regulation of osmotic stress transcription factor 1 (OSTF1) in tilapia during osmotic stress. Biochem Biophys Res Commun 426(3):294–298

    Google Scholar 

  77. Rengmark A, Slettan A, Lee W, Lie Ø, Lingaas F (2007) Identification and mapping of genes associated with salt tolerance in tilapia. J Fish Biol 71:409–422

    Google Scholar 

  78. Fiol DF, Sanmarti E, Lim AH, Kültz D (2011) A novel GRAIL E3 ubiquitin ligase promotes environmental salinity tolerance in euryhaline tilapia. BBA-Gen Subjects 1810:439–445

    Google Scholar 

Download references

Acknowledgments

This work was supported by Shanghai Educational Development Foundation (12CG56 to B.Y.), Research Award Fund in Shanghai Ocean University ( A-2400-12-0000-418 to B.Y.), Shanghai cultivation fund for Outstanding Young Teachers (B-5409-11-0012 to Z.-H.W. ), and China Agriculture Research System (CARS-49-04B to J.-L.Z.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhen-Hua Wang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yan, B., Wang, ZH. & Zhao, JL. Mechanism of osmoregulatory adaptation in tilapia. Mol Biol Rep 40, 925–931 (2013). https://doi.org/10.1007/s11033-012-2133-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-012-2133-7

Keywords

Navigation