Skip to main content
SpringerLink
Log in

Alanine and taurine transport by the gill epithelium of a marine bivalve: Effect of sodium on influx

  • Articles
  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

Marine mussels can accumulate amino acids from seawater into the epithelial cells of the gill against chemical gradients in excess of 5×106 to 1. Uptake of both alanine and taurine into gill tissue isolated fromMytilus californianus was found to be dependent upon Na+ in the external solution. Uptake of these amino acids was described by Michaelis-Menten kinetics, and a reduction in external [Na+] (from 425 to 213mm) increased the apparent Michaelis constants (alanine, from 8 to 17 μm; taurine, from 4 to 39 μm) without a significant influence on theJ max's of these processes. Fivemm harmaline, an inhibitor of Na-cotransport processes in many systems, reduced both alanine and taurine uptake by more than 95%; this inhibition appeared to be competitive in nature, with an apparentK i of 43 μm for the interaction with alanine uptake. Increasing the external [Na+] from 0 to 510mm produced a sigmoid activation of alanine and taurine uptake withK Na's of approximately 325mm. The apparent Hill coefficients for this activation were 7.3 and 7.4 for alanine and taurine, respectively. These data are consistent with uptake mechanisms which require comparatively high concentrations of Na+ to activate transport, and which couple several Na+ ions to the transport of each amino acid. These characteristics, in conjunction with the previously demonstrated low passive permeability of the apical membrane to amino acids, result in systems capable of i) accumulating amino acids from seawater to help meet the nutritional needs of this animal, and ii) maintaining the high intracellular amino-acid concentrations associated with volume regulation in the gill.

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

Similar content being viewed by others

References

  1. Aiello, E.L. 1970. Nervous and chemical stimulation of the gill cilia in bivalve molluscs.Physiol. Zool. 43:60–70

    Google Scholar 

  2. Anderson, J.W. 1975. The uptake and incorporation of glycine by the gills ofRangia cuneata (Mollusca: Bivalvia) in response to variations in salinity and sodium.In: Physiological Ecology of Estuarine Organisms. F.J. Vernberg, editor. pp. 239–258. University of South Carolina Press Columbia, South Carolina

    Google Scholar 

  3. Aronson, P.S. 1981. Identifying secondary active solute transport in epithelia.Am. J. Physiol. 240:F1-F11

    PubMed  Google Scholar 

  4. Aronson, P.S., Bounds, S.E. 1980. Harmaline inhibition of Na-dependent transport in renal microvillus membrane vesicles.Am. J. Physiol. 238:F210-F217

    PubMed  Google Scholar 

  5. Cavanaugh, G.M. 1956. Formulae and Methods, IV, of the Marine Biological Laboratory Chemical Room. Marine Biological Laboratory, Woods Hole, Massachusetts

    Google Scholar 

  6. Christensen, H.N., De Cespedes, C., Handlogten, M.E., Ronquist, G. 1973. Energization of amino acid transport, studied for the Ehrlich ascites cell.Biochim. Biophys. Acta 300:487–522

    PubMed  Google Scholar 

  7. Christensen, H.N., Hess, N., Riggs, T.R. 1954. Concentration of taurine, β-alanine, and tri-iodothyronine by ascites tumor cells.Cancer Res. 14:124–127

    PubMed  Google Scholar 

  8. Crane, R.K. 1977. The gradient hypothesis and other models of carrier mediated active transport.Rev. Physiol. Biochem. Pharmacol. 78:101–163

    Google Scholar 

  9. Crowe, J.H. 1981. Transport of exogenous substrate and cell volume regulation in bivalve molluscs.J. Exp. Zool. 215:363–370

    Google Scholar 

  10. Curran, P.F., Schultz, S.G., Chez, R.A., Fuisz, R.E. 1967. Kinetic relations of Na-amino acid interaction at the mucosal border of intestine.J. Gen. Physiol. 50:1261–1286

    PubMed  Google Scholar 

  11. Duggleby, R.G. 1981. A nonlinear regression program for small computers.Anal. Biochem. 110:9–18

    PubMed  Google Scholar 

  12. Gerenscer, G.A. 1983. Na+ absorption inAplysia intestine: Na+ fluxes and intracellular Na+ and K+ activities.Am. J. Physiol. 244:R412-R417

    PubMed  Google Scholar 

  13. Gilles, R. 1979. Intracellular organic osmotic effectors.In: Mechanisms of Osmoregulation in Animals. R. Gilles, editor. pp. 111–154. John Wiley & Sons, New York

    Google Scholar 

  14. Gomme, J. 1982. Laminar water flow, amino acid absorption, and amino acid recycling in the mussel gill.Am. Zool. 22:989

    Google Scholar 

  15. Heinz, A., Jackson, J.W., Rickey, B.E., Sachs, G., Schafer, J.A. 1981. Amino acid active transport and stimulation by substrates in the absence of a Na+ electrochemical potential gradient.J. Membrane Biol. 62:149–160

    Google Scholar 

  16. Jørgensen, C.B. 1983. Patterns of uptake of dissolved amino acids in mussels (Mytilus edulis).Mar. Biol. 73:177–182

    Google Scholar 

  17. Kaunitz, J.D., Gunther, R., Wright, E.M. 1982. Involvement of multiple sodium ions in intestinal D-glucose transport.Proc. Natl. Acad. Sci. USA 79:2315–2318

    PubMed  Google Scholar 

  18. Kimmich, G.A. 1981. Gradient coupling in isolated intestinal cells.Fed. Proc. 40:2474–2479

    PubMed  Google Scholar 

  19. Kimmich, G.A., Randles, J. 1980. Evidence for an intestinal Na+: sugar transport coupling stoichiometry of 2.0.Biochim. Biophys. Acta 596:439–444

    PubMed  Google Scholar 

  20. Kinsella, J.L., Aronson, P.S. 1980. Properties of the Na+−H+ exchanger in renal microvillus membrane vesicles.Am. J. Physiol. 238:F461-F469

    PubMed  Google Scholar 

  21. Lange, R. 1963. The osmotic function of amino acids and taurine in the mussel,Mytilus edulis.Comp. Biochem. Physiol. 10:173–179

    PubMed  Google Scholar 

  22. Love, R.D., Uglem, G.L. 1978. Estimation of the coupling coefficient for glucose and sodium transport inHymenolepis diminuta.J. Parisitol. 64:426–430

    Google Scholar 

  23. Murakami, A., Takahashi, K. 1975. Correlation of electrical and mechanical responses in nervous control of cilia.Nature (London) 257:48–49

    Google Scholar 

  24. Péquignat, E. 1973. A kinetic and autoradiographic study of the direct assimilation of amino acids and glucose by organs of the musselMytilus edulis.Mar Biol. 19:227–244

    Google Scholar 

  25. Preston, R.L., Stevens, B.R. 1982. Kinetic and thermodynamic aspects of sodium-coupled amino acid transport by marine invertebrates.Am. Zool. 22:709–721

    Google Scholar 

  26. Sacchi, V.F., Hanozet, G.M., Giordana, B. 1984. α-Aminoisobutyric acid transport in the midgut of two lepidopteran larvae.J. Exp. Biol. 108:329–339

    Google Scholar 

  27. Segel, I.H. 1975. Enzyme Kinetics. John Wiley & Sons, New York

    Google Scholar 

  28. Stein, W.D. 1967. The Movement of Molecules Across Cell Membranes. Academic, New York

    Google Scholar 

  29. Stevens, B.R., Preston, R.L. 1980. The effect of sodium on the kinetics ofl-alanine influx by the integument of the marine polychaeteGlycera dibranchiata J. Exp. Zool. 211:129–138

    Google Scholar 

  30. Stewart, M.G., Bamford, D.R. 1975. Kinetics of alanine uptake by the gills of the soft shelled clamMya arenaria.Comp. Biochem. Physiol. 52A:67–74

    Google Scholar 

  31. Turner, R.J., Moran, A. 1982. Further studies of proximal tubular brush border membraned-glucose transport heterogeneity.J. Membrane Biol. 70:37–45

    Google Scholar 

  32. Vidaver, G.A. 1964. Some tests of the hypothesis that the sodium-ion gradient furnishes the energy for glycine-active transport by pigeon red cells.Biochemistry 6:803–808

    Google Scholar 

  33. Wright, E.M., Wright, S.H., Hirayama, B., Kippen, I. 1982. Interactions between lithium and renal transport of Krebs cycle intermediates.Proc. Natl. Acad. Sci. USA 79:7514–7517

    PubMed  Google Scholar 

  34. Wright, S.H. 1979. Effect of activity of lateral cilia on transport of amino acids in gills ofMytilu californianus.J. Exp. Zool. 209:209–220

    Google Scholar 

  35. Wright, S.H. 1982. A nutritional role for amino acid transport in filter-feeding marine invertebrates.Am. Zool. 22:621–634

    Google Scholar 

  36. Wright, S.H. 1985. Multiple pathways for amino acid transport inMytilus gill.J. Comp. Physiol. 156:259–267

    Google Scholar 

  37. Wright, S.H., Kippen, I., Wright, E.M. 1982. Stoichiometry of Na+-succinate cotransport in renal brush-border membranes.J. Biol. Chem. 257:1773–1778

    PubMed  Google Scholar 

  38. Wright, S.H., Secomb, T.W. 1984. Epidermal taurine transport in marine mussels.Am. J. Physiol. 247:R346-R355

    PubMed  Google Scholar 

  39. Wright, S.H., Secomb, T.W. 1986. Epithelial amino acid transport in marine mussels: Role in net exchange of taurine between gills and sea water.J. Exp. Biol. 121:251–270

    Google Scholar 

  40. Wright, S.H., Southwell, K.M., Stephens, G.C. 1984. Autoradiographic analysis of amino acid uptake by the gill ofMytilus.J. Comp Physiol. 154:249–256

    Google Scholar 

  41. Wright, S.H., Stephens, G.C. 1977. Characteristics of influx and net flux of amino acids inMytilus californianus.Biol. Bull. 152:295–310

    PubMed  Google Scholar 

  42. Zurburg, W., De Zwaan, A. 1981. The role of amino acids in anaerobiosis and osmoregulation in bivalves.J. Exp. Zool. 215:315–325

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology, College of Medicine, University of Arizona, 85724, Tucson, Arizona

    Stephen H. Wright

Authors
  1. Stephen H. Wright
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wright, S.H. Alanine and taurine transport by the gill epithelium of a marine bivalve: Effect of sodium on influx. J. Membrain Biol. 95, 37–45 (1987). https://doi.org/10.1007/BF01869628

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01869628

Key Words

Search

Navigation