Exposure to pH 3.5 water has no effect on the gills of the Amazonian tambaqui (Colossoma macropomum)

Abstract

Tambaqui (Colossoma macropomum) are a model species for tropical fish physiology, but details are lacking about their ionoregulatory response to acid waters. To provide specifics, we measured unidirectional Na+ fluxes in low pH waters. Sodium influx (\(J_{{{\text{in}}}}^{{{\text{Na}}}}\)) was uninhibited during acute exposure to pH 4.5 and 3.5, and Na efflux (\(J_{{{\text{out}}}}^{{{\text{Na}}}}\)) rose only slightly at pH 3.5; net Na+ flux (\(J_{{{\text{net}}}}^{{{\text{Na}}}}\)) remained positive at all pH. Similarly, during 24 h transfer to pH 3.5 \(J_{{{\text{in}}}}^{{{\text{Na}}}}\), \(J_{{{\text{out}}}}^{{{\text{Na}}}}\), and \(J_{{{\text{net}}}}^{{{\text{Na}}}}\) were unchanged at all times. Taking a closer look at the mechanism of Na+ transport in the gills of tambaqui we found that \(J_{{{\text{in}}}}^{{{\text{Na}}}}\) was uninhibited by HMA, a Na+/H+-exchanger blocker, and Benzamil, a Na+-channel inhibitor, casting doubt on their role in Na+ uptake in this fish. Measurement of Na+/K+-ATPase (NKA) and H+-ATPase (VHA) activity showed that neither changed at low pH compared to measurements at pH 6.5. Western blot analysis of ATPase expression saw no changes in amount of NKA and VHA at low pH, and immunohistochemistry showed expression of both NKA and VHA on lamellae and interlamellar region of tambaqui gills and that both proteins co-localized to the same gill cells. Location of expression also did not change in low pH water. Amazingly, tambaqui seem unaffected by pH 3.5 water, making them one of the most acid-tolerant fish species examined so far. In addition, they appear to share key ionoregulatory traits with other fish of the order Characiformes, which suggest a common origin for the ionoregulatory attributes.

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References

  1. Araújo JD, Ghelfi A, Val AL (2017) Triportheus albus Cope, 1872 in the blackwater, clearwater, and whitewater of the Amazon: a case of phenotypic plasticity? Front Genet 8:1–12

    Article  Google Scholar 

  2. Aride PHR, RoubachVal RAL (2007) Tolerance response of Tambaqui Colossoma macropomum (Cuvier) to water pH. Aquat Res 38:588–594

    CAS  Article  Google Scholar 

  3. Arroyave J, Denton JSS, Stiassny MLJ (2013) Are characiform fishes Gondwanan in origin? Insights from time-scaled molecular phylogeny of the Citharinoidei (Ostariophysi: Characiformes). PLoS ONE 8:1–24

    Article  Google Scholar 

  4. Betancur-Rodriguez R, Wiley EO, Arriata G, Acero A, Bailly N, Miya M, Lecointre G, Orti G (2017) Phylogenetic classification of bony fishes. BMC Evol Biol 17:162

    Article  Google Scholar 

  5. Duarte FM, Feirrera MS, Wood CM, Val AL (2013) Effect of low pH exposure on Na+ regulation in two cichlid species of the Amazon. Comp Biochm Physiol A 166:441–448

    CAS  Article  Google Scholar 

  6. Dymowska AK, Schultz AG, Blair SD, Chamot D, Goss GG (2014) Acid-sensing ion channels are involved in epithelial Na+ uptake in the rainbow trout Oncorhynchus mykiss. Am J Physiol Cell Physiol 307:C255–C265

    CAS  Article  Google Scholar 

  7. Dymowska AK, Boyle D, Schultz AG, Goss GG (2015) The role of acid-sensing ion channels in epithelial Na+ uptake in adult zebrafish (Danio rerio). J Exp Biol 218:1244–1251

    Article  Google Scholar 

  8. Fambrough DM (1989) Molecular characterization and expression of the (Na+ + K+)-ATPase alpha-subunit in Drosophila melanogaster. EMBO J 8:193–202

    Article  Google Scholar 

  9. Filippova M, Ross LS, Gill SS (1998) Cloning of the V-ATPase B subunit cDNA from Culex quinquefasciatus and expression of the B and C subunits in mosquitoes. Insect Mol Biol 7:223–232

    CAS  Article  Google Scholar 

  10. Florindo LH, Leite CA, Kalinin AL, Reid SG, Milsom WK, Rantin FT (2006) The role of branchial and orobranchial O2 chemoreceptors in the control of aquatic surface respiration in the neotropical fish Tambaqui (Colossoma macropomum): progressive responses to prolonged hypoxia. J Exp Biol 209:1709–1715

    Article  Google Scholar 

  11. Freda J, McDonald DG (1988) Physiological correlates of interspecific variation in acid tolerance in fish. J Exp Biol 136:243–258

    CAS  Google Scholar 

  12. Furch K (1984) Water chemistry of the Amazon basin: the distribution of chemical elements among freshwaters. In: Sioli H (ed) The Amazon. Limnology and landscape ecology of a mighty tropical river and its basin. Dr. W. Junk Publishers, Dordrecht, pp 167–199

    Google Scholar 

  13. Gaillardet J, Dupre B, Allegre CJ, Negrel P (1997) Chemical and physical denudation in the Amazon River Basin. Chem Geol 142:141–173

    CAS  Article  Google Scholar 

  14. Gonzalez RJ, Cradeur A, GuinnipMitchellReduta MAV (2018) South American Characids share very similar ionoregulatory characteristics. Comp Biochem Physiol A 226:17–21

    CAS  Article  Google Scholar 

  15. Gonzalez RJ, Dalton VM, Patrick ML (1997) Ion regulation in ion-poor, acidic water by the blackskirt tetra (Gymnocorymbus ternetzi), a fish native to the Amazon River. Physiol Zool 70:428–435

    CAS  Article  Google Scholar 

  16. Gonzalez RJ, Dunson WA (1987) Adaptations of sodium balance to low pH in a sunfish (Enneacanthus obesus) from naturally acidic waters. J Comp Physiol B 157:555–566

    Article  Google Scholar 

  17. Gonzalez RJ, Dunson WA (1989) Acclimation of sodium regulation to low pH and the role of calcium in the acid-tolerant sunfish Enneacanthus obesus. Physiol Zool 62:977–992

    Article  Google Scholar 

  18. Gonzalez RJ, Jones SL, Nguyen TV (2017) Ionoregulatory characteristics of non-Rio Negro Characiforms and Cichlids. Physiol Biochem Zool 90:407–414

    CAS  Article  Google Scholar 

  19. Gonzalez RJ, Preest M (1999) Mechanisms for exceptional tolerance of ion-poor, acidic waters in the neon tetra (Paracheirodon innesi). Physiol Biochem Zool 72:156–163

    CAS  Article  Google Scholar 

  20. Gonzalez RJ, Wilson RW (2001) Patterns of ion regulation in acidophilic fish native to the ion-poor, acidic Rio Negro. J Fish Biol 58:1680–1690

    Article  Google Scholar 

  21. Gonzalez RJ, Wilson RW, Wood CM (2005) Ionoregulation in tropical fish from ion-poor, acidic blackwaters. In: Val AL, Val VMFA, Randall DJ (eds) The physiology of tropical fishes. Fish physiology series, vol 21. Academic Press, San Diego, pp 397–442

    Google Scholar 

  22. Gonzalez RJ, Wood CM, Wilson RW, Patrick ML, Val AL (2002) Diverse strategies of ion regulation in fish collected from the Rio Negro. Physiol Biochem Zool 75:37–47

    CAS  Article  Google Scholar 

  23. Goulding M (1980) The fishes and the forest: explorations in Amazonian natural history. University of California Press, Berkeley

    Google Scholar 

  24. Goulding M, Carvalho ML (1982) Life history and management of the Tambaqui (Colossoma macropomum, Characidae): an important Amazonian food fish. Rev Bras Zool 1:107–133

    Article  Google Scholar 

  25. Jagoe CH, Haines TA (1990) Morphometric effects of low pH and limed water on the gills of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 47:2451–2460

    Article  Google Scholar 

  26. Kaneko T, Hasegawa S, Uchida K, Ogasawara T, Oyagi A, Hirano T (1999) Acid tolerance of Japanese Dace (a Cyprinid Teleost) in Lake Osorezan, a Remarkable Acid Lake. Zool Sci 16:871–877

    Article  Google Scholar 

  27. Kultz DR, Somero GN (1995) Osmotic and thermal effects on in situ ATPase activity in permeabilized gill epithelial cells of the fish Gillichthys mirabilis. Journ Exp Biol 198:1883–1894

    Google Scholar 

  28. Leino RL, McCormick JH, Jensen KM (1987) Changes in gill histology of fathead minnows and yellow perch transferred to soft water or acidified soft water with particular reference to chloride cells. Cell Tissue Res 250:389–399

    Article  Google Scholar 

  29. Maetz J, Garcia-Romeu F (1964) The mechanism of sodium and chloride uptake by the gills of a fresh-water fish, Carassius auratus II. Evidence for NH4+/Na+ and HCO3/Cl exchanges. J Gen Physiol 47:1209–1227

    CAS  Article  Google Scholar 

  30. McDonald DG, Freda J, Cavdek V, Gonzalez R, Zia S (1991) Interspecific differences in gill morphology of freshwater fish in relation to tolerance of low-pH environments. Physiol Zool 64:124–144

    Article  Google Scholar 

  31. Perry SF (1986) Carbon dioxide excretion in fishes. Can J Zool 64:565–572

    Article  Google Scholar 

  32. Preest M, Gonzalez RJ, Wilson RW (2005) A pharmacological examination of the Na+ and Cl- transport mechanisms in freshwater fish. Physiol Biochem Zool 78:259–272

    CAS  Article  Google Scholar 

  33. Roubach R, Saint-Paul U (1994) Use of fruits and seeds from Amazonian inundated forests in feeding trials with Colossoma macropomum (Cuvier, 1818) (Pisces, Characidae). J Appl Ichthyol 10:134–140

    Article  Google Scholar 

  34. Saint-Paul U (1984) Physiological adaptation to hypoxia of a neotropical characoid fish Colossoma macropomum. Serrasalmidae Environ Biol Fish 11:53–62

    Article  Google Scholar 

  35. Val AL, de Almeida-Val VMF (1995) Fishes of the Amazon and their environment. Springer, Berlin

    Google Scholar 

  36. Wilson RW, Wood CM, Gonzalez RJ, Patrick ML, Bergman H, Narahara A, Val AL (1999) Net ion fluxes during gradual acidification of extremely soft water in three species of Amazonian fish. Physiol Biochem Zool 72:277–285

    CAS  Article  Google Scholar 

  37. Wood CM, de Souza Netto JG, Wilson JM, Duarte RM, Val AL (2017) Nitrogen metabolism in Tambaqui (Colossoma macropomum), a neotropical model teleost: hypoxia, temperature, exercise, feeding, fasting, and high environmental ammonia. J Comp Physiol B 186:431–445

    Article  Google Scholar 

  38. Wood CM, Gonzalez RJ, Ferreira MS, Mota SB, Val AL (2018) The physiology of the Tambaqui (Colossoma macropomum) at pH 8.0. J Comp Physiol B 188:393–408

    Article  Google Scholar 

  39. Wood CM, Robertson LM, Johannsson OE, Val AL (2014) Mechanisms of Na+ uptake, ammonia excretion and their potential linkage in native Rio Negro tetras (Paracheirodon axelrodi, hemigrammus rhodostomus, and Moenkhausia diktyota). J Comp Physiol B 187:877–890

    Article  Google Scholar 

  40. Wood CM, Wilson RW, Gonzalez RJ, Patrick ML, Bergman H, Narahara A, Val AL (1998) Responses of an Amazonian teleost, the tambaqui (Colossoma macropomum) to low pH in extremely soft water. Physiol Zool 71:658–670

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work was funded by University of San Diego Faculty Research Grants to RJG and MLP. Travel to Manaus was funded by University of San Diego International Travel Grants. Financial support by INCT ADAPTA–CNPq(465540/2014-7)/FAPEAM (062.1187/2017)/CAPES(finance code 001). ALV is the recipient of a research fellowship from Brazilian CNPq.

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Gonzalez, R.J., Patrick, M.L., Duarte, R.M. et al. Exposure to pH 3.5 water has no effect on the gills of the Amazonian tambaqui (Colossoma macropomum). J Comp Physiol B (2021). https://doi.org/10.1007/s00360-021-01349-x

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Keywords

  • Fish
  • Ion regulation
  • Low pH