Advertisement

Journal of Comparative Physiology B

, Volume 182, Issue 2, pp 259–274 | Cite as

Compensatory regulation of acid–base balance during salinity transfer in rainbow trout (Oncorhynchus mykiss)

  • K. M. Gilmour
  • S. F. Perry
  • A. J. Esbaugh
  • J. Genz
  • J. R. Taylor
  • M. Grosell
Original Paper

Abstract

In seawater-acclimated rainbow trout (Oncorhynchus mykiss), base secretion into the intestine is a key component of the intestinal water absorption that offsets osmotic water loss to the marine environment. Acid–base balance is maintained by the matched excretion of acid equivalents via other routes, presumably the gill and/or kidney. The goal of the present study was to examine acid–base balance in rainbow trout upon transfer to more dilute environments, conditions under which base excretion into the intestine is predicted to fall, requiring compensatory adjustments of acid excretion at the gill and/or kidney if acid–base balance is to be maintained. Net acid excretion via the gill/kidney and rectal fluid, and blood acid–base status were monitored in seawater-acclimated rainbow trout maintained in seawater or transferred to iso-osmotic conditions. As predicted, transfer to iso-osmotic conditions significantly reduced base excretion into the rectal fluid (by ~48%). Transfer to iso-osmotic conditions also significantly reduced the excretion of titratable acidity via extra-intestinal routes from 183.4 ± 71.3 to −217.5 ± 42.7 μmol kg−1 h−1 (N = 7). At the same time, however, ammonia excretion increased significantly during iso-osmotic transfer (by ~72%) so that the apparent overall reduction in net acid excretion (from 419.7 ± 92.9 to 189.2 ± 76.5 μmol kg−1 h−1; N = 7) was not significant. Trout maintained blood acid–base status during iso-osmotic transfer, although arterial pH was significantly higher in transferred fish than in those maintained in seawater. To explore the mechanisms underlying these adjustments of acid–base regulation, the relative mRNA expression and where possible, activity of a suite of proteins involved in acid–base balance were examined in intestine, gill and kidney. At the kidney, reduced mRNA expression of carbonic anhydrase (CA; cytosolic and membrane-associated CA IV), V-type H+-ATPase, and Na+/HCO3 co-transporter were consistent with a reduced role in net acid excretion following iso-osmotic transfer. Changes in relative mRNA expression and/or activity at the intestine and gill were consistent with the roles of these organs in osmotic rather than acid–base regulation. Overall, the data emphasize the coordination of acid–base, osmoregulatory and ionoregulatory processes that occur with salinity transfer in a euryhaline fish.

Keywords

Intestinal base secretion Acid–base regulation Gill Kidney Salinity transfer Rainbow trout Ion transporters Carbonic anhydrase 

Notes

Acknowledgments

This study was supported by Natural Sciences and Engineering Research Council (NSERC) of Canada Discovery and Research Tools and Instruments grants to KMG and SFP, and a National Science Foundation (NSF) grant (IAB 0743903) to MG. JRT and JG received Journal of Experimental Biology Travelling Fellowships, and AJE was supported by an NSERC Postdoctoral Fellowship. The help of Branka Vulesevic was greatly appreciated. We are grateful to Mr. Ray Volk and Mr. Steven Emmonds of the Robertson Creek Hatchery (Department of Fisheries and Oceans, Port Alberni, BC, Canada) for their help in supplying the trout used for this study. Mr. Randy Dolighan (British Columbia Ministry of Environment, Nanaimo, BC, Canada) is thanked for providing the brood stock from which the trout used in the study were derived. The enthusiasm and tireless support of Dr. Bruce Cameron (BMSC Research Director) were invaluable—thank you.

References

  1. Ando M, Subramanyam MVV (1990) Bicarbonate transport systems in the intestine of the seawater eel. J Exp Biol 150:381–394Google Scholar
  2. Bath RN, Eddy FB (1979) Ionic and respiratory regulation in rainbow trout during rapid transfer to seawater. J Comp Physiol 134:351–357CrossRefGoogle Scholar
  3. Beyenbach KW (2004) Kidneys sans glomeruli. Am J Physiol 286:F811–F827CrossRefGoogle Scholar
  4. Boutilier RG, Heming TA, Iwama GK (1984) Appendix: Physicochemical parameters for use in fish respiratory physiology. In: Hoar WS, Randall DJ (eds) Fish Physiology. Academic Press, Inc., London, pp 403–430Google Scholar
  5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utlizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  6. Brown JA, Oliver JA, Henderson IW, Jackson BA (1980) Angiotensin and single nephron glomerular function in the trout Salmo gairdneri. Am J Physiol 239:R509–R514PubMedGoogle Scholar
  7. Buxton TB, Crockett JK, Moore WL 3rd, Moore WL Jr, Rissing JP (1979) Protein precipitation by acetone for the analysis of polyethylene glycol in intestinal perfusion fluid. Gastroenterology 76:820–824PubMedGoogle Scholar
  8. Bystriansky JS, Richards JG, Schulte PM, Ballantyne JS (2006) Reciprocal expression of gill Na+/K+-ATPase α-subunit isoforms α1a and α1b during seawater acclimation of three salmonid fishes that vary in their salinity tolerance. J Exp Biol 209:1848–1858PubMedCrossRefGoogle Scholar
  9. Claiborne JB, Edwards SL, Morrison-Shetlar AI (2002) Acid-base regulation in fishes: cellular and molecular mechanisms. J Exp Zool 293:302–319PubMedCrossRefGoogle Scholar
  10. Cliff WH, Beyenbach KW (1992) Secretory renal proximal tubules in seawater- and freshwater-adapted killifish. Am J Physiol 262:F116Google Scholar
  11. Colin DA, Nonnotte G, LeRay C, Nonnotte L (1985) Na transport and enzyme activities in the intestine of the freshwater and sea-water adapted trout (Salmo gairdnerii R.). Comp Biochem Physiol 81A:695–698CrossRefGoogle Scholar
  12. Cooper CA, Whittamore JM, Wilson RW (2010) Ca2+-driven intestinal HCO3 secretion and CaCO3 precipitation in the European flounder in vivo: influences on acid-base regulation and blood gas transport. Am J Physiol 298:R870–R876CrossRefGoogle Scholar
  13. Evans RM (1979) Onset and rate of drinking in rainbow trout (Salmo gairdneri) following transfer to dilute seawater. Can J Zool 57:1863–1865CrossRefGoogle Scholar
  14. 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 85:97–177PubMedCrossRefGoogle Scholar
  15. Fuentes J, Bury NR, Carroll S, Eddy FB (1996a) Drinking in Atlantic salmon presmolts (Salmo salar L.) and juvenile rainbow trout (Oncorhynchus mykiss Walbaum) in response to cortisol and sea water challenge. Aquaculture 141:129–137CrossRefGoogle Scholar
  16. Fuentes J, Soengas JL, Buceta M, Otero J, Rey P, Rebolledo E (1996b) Kidney ATPase response in seawater-transferred rainbow trout (Oncorhynchus mykiss). Effect of salinity and fish size. J Physiol Biochem 52:231–238Google Scholar
  17. Fuentes J, Soengas JL, Rey P, Rebolledo E (1997) Progressive transfer to seawater enhances intestinal and branchial Na+-K+-ATPase activity in non-anadromous rainbow trout. Aquac Int 5:217–227CrossRefGoogle Scholar
  18. Gaumet F, Boeuf G, Truchot J-P, Nonnotte G (1994) Effects of environmental water salinity on blood acid-base status in juvenile turbot (Scophthalmus maximus L.). Comp Biochem Physiol 109A:985–994CrossRefGoogle Scholar
  19. Genz J, Taylor JR, Grosell M (2008) Effects of salinity on intestinal bicarbonate secretion and compensatory regulation of acid-base balance in Opsanus beta. J Exp Biol 211:2327–2335PubMedCrossRefGoogle Scholar
  20. Georgalis T, Gilmour KM, Yorston J, Perry SF (2006) The roles of cytosolic and membrane bound carbonic anhydrase in the renal control of acid-base balance in rainbow trout Oncorhynchus mykiss. Am J Physiol 291:F407–F421CrossRefGoogle Scholar
  21. Grosell M (2006) Intestinal anion exchange in marine fish osmoregulation. J Exp Biol 209:2813–2827PubMedCrossRefGoogle Scholar
  22. Grosell M (2011). Intestinal anion exchange in marine teleosts is involved in osmoregulation and contributes to the oceanic inorganic carbon cycle. Acta Physiol (in press)Google Scholar
  23. Grosell M, Genz J (2006) Ouabain-sensitive bicarbonate secretion and acid absorption by the marine teleost fish intestine play a role in osmoregulation. Am J Physiol 291:R1145–R1156Google Scholar
  24. Grosell M, Taylor JR (2007) Intestinal anion exchange in teleost water balance. Comp Biochem Physiol A 148:14–22Google Scholar
  25. Grosell M, Wood CM, Wilson RW, Bury NR, Hogstrand C, Rankin JC, Jensen FB (2005) Bicarbonate secretion plays a role in chloride and water absorption of the European flounder intestine. Am J Physiol 288:R936–R946Google Scholar
  26. Grosell M, Gilmour KM, Perry SF (2007) Intestinal carbonic anhydrase, bicarbonate- and proton carriers play a role in the acclimation of rainbow trout to seawater. Am J Physiol 293:R2099–R2111Google Scholar
  27. Grosell M, Genz J, Taylor JR, Perry SF, Gilmour KM (2009a) The involvement of H+-ATPase and carbonic anhydrase in intestinal HCO3 secretion in seawater-acclimated rainbow trout. J Exp Biol 212:1940–1948PubMedCrossRefGoogle Scholar
  28. Grosell M, Mager EM, Willisams C, Taylor JR (2009b) High rates of HCO3 secretion and Cl absorption against adverse gradients in the marine teleost intestine: the involvement of an electrogenic anion exchanger and H+-pump metabolon? J Exp Biol 212:1684–1696PubMedCrossRefGoogle Scholar
  29. Henry RP (1991) Techniques for measuring carbonic anhydrase activity in vitro: the electrometric delta pH and pH stat assays. In: Dodgson SJ, Tashian RE, Gros G, Carter ND (eds) The carbonic anhydrases: cellular physiology and molecular genetics. Plenum, New York, pp 119–126Google Scholar
  30. Hickman CP Jr, Trump BF (1969) The kidney. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol. 1. Academic Press, New York, pp 91–239Google Scholar
  31. Holmes RM (1961) Kidney function in migrating salmonids. Rep Challenger Soc Camb 3:23Google Scholar
  32. Ivanis G, Braun M, Perry SF (2008a) Renal expression and localization of SLC9A3 sodium/hydrogen exchanger and its possible role in acid-base regulation in freshwater rainbow trout (Oncorhynchus mykiss). Am J Physiol 295:R971–R978CrossRefGoogle Scholar
  33. Ivanis G, Esbaugh A, Perry SF (2008b) Branchial expression and localization of SLC9A2 and SLC9A3 sodium/hydrogen exchangers and their possible role in acid-base regulation in freshwater rainbow trout (Oncorhynchus mykiss). J Exp Biol 211:2467–2477PubMedCrossRefGoogle Scholar
  34. Kurita Y, Nakada T, Kato A, Doi H, Mistry AC, Chang M-H, Romero MF, Hirose S (2008) Identification of intestinal bicarbonate transporters involved in formation of carbonate precipitates to stimulate water absorption in marine teleost fish. Am J Physiol 294:R1402–R1412Google Scholar
  35. Lin H, Randall DJ (1993) H+-ATPase activity in crude homogenates of fish gill tissue: inhibitor sensitivity and environmental and hormonal regulation. J Exp Biol 180:163–174Google Scholar
  36. Marshall WS (2002) Na+, Cl, Ca2+ and Zn2+ transport by fish gills: retrospective review and prospective synthesis. J Exp Zool 293:264–283PubMedCrossRefGoogle Scholar
  37. Marshall WS, Grosell M (2006) Ion transport, osmoregulation, and acid-base balance. In: Evans DH, Claiborne JB (eds) The physiology of fishes, 3rd edn. CRC Press, Boca Raton, pp 177–230Google Scholar
  38. McCormick SD (1993) Methods for nonlethal gill biopsy and measurement of Na+, K+-ATPase activity. Can J Fish Aquat Sci 50:656–658CrossRefGoogle Scholar
  39. McCormick SD (1995) Hormonal control of gill Na+, K+-ATPase and chloride cell function. In: Wood CM, Shuttleworth TJ (eds) Cellular and molecular approaches to fish ionic regulation. Academic Press, San Diego, pp 285–315Google Scholar
  40. McCormick SD, Regish AM, Christensen AK (2009) Distinct freshwater and seawater isoforms of Na+/K+-ATPase in gill chloride cells of Atlantic salmon. J Exp Biol 212:3994–4001PubMedCrossRefGoogle Scholar
  41. McDonald DG, Wood CM (1981) Branchial and renal acid and ion fluxes in the rainbow trout, Salmo gairdneri, at low environmental pH. J Exp Biol 93:101–118Google Scholar
  42. Nilsen TO, Ebbesson LOE, Madsen SS, McCormick SD, Andersson E, Björnsson BT, Prunet P, Stefansson SO (2007) Differential expression of gill Na+, K+-ATPase a- and ß-subunits, Na+, K+, 2Cl cotransporter and CFTR anion channel in juvenile anadromous and landlocked Atlantic salmon Salmo salar. J Exp Biol 210:2885–2896PubMedCrossRefGoogle Scholar
  43. Patrick M, Pärt P, Marshall WS, Wood CM (1997) Characterization of ion and acid-base transport in the fresh water adapted mummichog (Fundulus heteroclitus). J Exp Zool 279:208–219CrossRefGoogle Scholar
  44. Pelis RM, Renfro JL (2004) Role of tubular secretion and carbonic anhdyrase in vertebrate renal sulfate excretion. Am J Physiol 287:R491–R501Google Scholar
  45. Perrott MN, Grierson CE, Hazon N, Balment RJ (1992) Drinking behaviour in sea water and fresh water teleosts, the role of the renin-angiotensin system. Fish Physiol Biochem 10:161–168CrossRefGoogle Scholar
  46. Perry SF, Gilmour KM (2006) Acid-base balance and CO2 excretion in fish: Unanswered questions and emerging models. Respir Physiol Neurobiol 154:199–215PubMedCrossRefGoogle Scholar
  47. Perry SF, Beyers ML, Johnson DA (2000a) Cloning and molecular characterisation of the trout (Oncorhynchus mykiss) vacuolar H+-ATPase B subunit. J Exp Biol 203:459–470PubMedGoogle Scholar
  48. Perry SF, Dumont C, Johnson DA (2000b) A molecular investigation of the role of the branchial vacuolar H+-ATPase in acid-base balance and ionic regulation in rainbow trout (Oncorhynchus mykiss). Ion transfer across fish gills. Proceedings of an International Fish Physiology Symposium held July 23–27, 2000:29–44Google Scholar
  49. Perry SF, Furimsky M, Bayaa M, Georgalis T, Shahsavarani A, Nickerson JG, Moon TW (2003) Integrated responses of Na+/HCO3 cotransporters and V-type H+-ATPases in the fish gill and kidney during respiratory acidosis. Biochim Biophys Acta 1618:175–184PubMedCrossRefGoogle Scholar
  50. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45PubMedCrossRefGoogle Scholar
  51. Richards JG, Semple JW, Bystriansky JS, Schulte PM (2003) Na+/K+-ATPase α-isoform switching in gills of rainbow trout (Oncorhynchus mykiss) during salinity transfer. J Exp Biol 206:4475–4486PubMedCrossRefGoogle Scholar
  52. Scott GR, Schulte PM, Wood CM (2006) Plasticity of osmoregulatory function in the killifish intestine: drinking rates, salt and water transport, and gene expression after freshwater transfer. J Exp Biol 209:4040–4050PubMedCrossRefGoogle Scholar
  53. Shehadeh ZH, Gordon MS (1969) The role of the intestine in salinity adaptation of the rainbow trout, Salmo gairdneri. Comp Biochem Physiol 30:397–418CrossRefGoogle Scholar
  54. Smith HW (1930) The absorption and excretion of water and salts by marine teleosts. Am J Physiol 93:480–505Google Scholar
  55. Soivio A, Nynolm K, Westman K (1975) A technique for repeated sampling of the blood of individual resting fish. J Exp Biol 62:207–217Google Scholar
  56. Sullivan GV, Fryer JN, Perry SF (1995) Immunolocalization of proton pumps (H+-ATPase) in pavement cells of rainbow trout gill. J Exp Biol 198:2619–2629PubMedGoogle Scholar
  57. Sullivan GV, Fryer JN, Perry SF (1996) Localization of mRNA for the proton pump (H+-ATPase) and Cl/HCO3 exchanger in the rainbow trout gill. Can J Zool 74:2095–2103CrossRefGoogle Scholar
  58. Taylor JR, Mager EM, Grosell M (2010) Basolateral NBCe1 plays a rate-limiting role in transepithelial intestinal HCO3 secretion, contributing to marine fish osmoregulation. J Exp Biol 213:459–468PubMedCrossRefGoogle Scholar
  59. Verdouw H, van Echted CJA, Dekkers EMJ (1978) Ammonia determination based on indophenol formation with sodium salicylate. Water Res 12:399–402CrossRefGoogle Scholar
  60. Walsh PJ, Blackwelder P, Gill KA, Danulat E, Mommsen TP (1991) Carbonate deposits in marine fish intestines: a new source of biomineralization. Limnol Oceanogr 36:1227–1232CrossRefGoogle Scholar
  61. Wilson RW, Grosell M (2003) Intestinal bicarbonate secretion in marine teleost fish: source of bicarbonate, pH sensitivity, and consequences for whole animal acid-base and calcium homeostasis. Biochim Biophys Acta 1618:163–174PubMedCrossRefGoogle Scholar
  62. Wilson RW, Wright PM, Munger RS, Wood CM (1994) Ammonia excretion in freshwater rainbow trout (Oncorhynchus mykiss) and the importance of gill boundary layer acidification: lack of evidence for Na+/NH4 + exchange. J Exp Biol 191:37–58PubMedGoogle Scholar
  63. Wilson RW, Gilmour KM, Henry RP, Wood CM (1996) Intestinal base excretion in the seawater-adapted rainbow trout: a role in acid-base balance? J Exp Biol 199:2331–2343PubMedGoogle Scholar
  64. Wilson RW, Wilson JM, Grosell M (2002) Intestinal bicarbonate secretion by marine teleost fish: why and how? Biochim Biophys Acta 1566:182–193PubMedCrossRefGoogle Scholar
  65. Wood CM, Marshall WS (1994) Ion balance, acid-base regulation, and chloride cell function in the common killifish, Fundulus heteroclitus: a euryhaline estuarine teleost. Estuaries 17:34–52CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • K. M. Gilmour
    • 1
    • 4
  • S. F. Perry
    • 1
    • 4
  • A. J. Esbaugh
    • 2
    • 4
  • J. Genz
    • 2
    • 4
  • J. R. Taylor
    • 3
    • 4
  • M. Grosell
    • 2
    • 4
  1. 1.Department of BiologyUniversity of OttawaOttawaCanada
  2. 2.RSMASUniversity of MiamiMiamiUSA
  3. 3.Monterey Bay Aquarium Research InstituteMontereyUSA
  4. 4.Bamfield Marine Sciences CentreBamfieldCanada

Personalised recommendations