Planta

, Volume 191, Issue 1, pp 34–40 | Cite as

Bicarbonate uptake in the marine macroalga Ulva sp. is inhibited by classical probes of anion exchange by red blood cells

  • Zivia Drechsler
  • Rajach Sharkia
  • Z. Ioav Cabantchik
  • Sven Beer
Article

Abstract

We demonstrate in this work that HCOinf3sup−uptake in the marine macroalga Ulva sp. features functional resemblances to anion transport mediated by anion exchangers of mammalian cell membranes. The evidence is based on (i) competitive inhibition of photosynthesis by the classical red-blood-cell anion-exchange blockers 4,4′-dinitrostilbene-2,2′-disulfonate and 4-nitro-4′-isothiocyanostilbene-2,2′-disulfonate under conditions where HCOinf3sup−, but not CO2, was the inorganic carbon form taken up; (ii) inhibition of HCOinf3uptake by pyridoxal phospate, indicating the involvement of lysine residues in the binding/translocation of HCOinf3sup−; and (iii) inhibition of HCOinf3sup−(but not of CO2) uptake by exofacial trypsin treatments, indicating the functional involvement of a plasmalemma protein. It is suggested that HCOinf3sup−uptake mediated by such a putative anion transporter can be a fundamental step in providing inorganic carbon for the CO2-concentrating system of marine marcoalgae in an environment where the HCOinf3sup−concentration is high, but the CO2 concentration and rates of uncatalyzed HCOinf3sup−dehydration are low.

Key words

Anion exchange(r) (band 3) protein Bicarbonate uptake Photosynthesis Protein (band 3) Ulva(photosynthesis) 

Abbreviations

CI

ionorganic carbon

DIDS

4,4′-diisothiocyanostilbene-2,2′-disulfonate

DNDS

4,4′-dinitrostilbene-2,2′-disulfonate

NIDS

4-nitro-4′-isothiocyanostilbene-2,2′-disulfonate

PLP

pyridoxal phosphate

Rubisco

ribulose-1,5-bisphosphate carboxylase-oxygenase

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References

  1. Alper, S.L. (1991) The band 3-related anion exchanger (AE) family. Annu. Rev. Physiol 53, 549–564Google Scholar
  2. Axelsson, L., Uusitalo, J. (1988) Carbon acquisition strategies for marine algae. I. Utilization of proton exchange visualized during photosynthesis in a closed system. Mar. Biol. 97, 295–300Google Scholar
  3. Badger, M.R., Price, G.D. (1992) The CO2 concentrating mechanism in cyanobacteria and microalgae. Physiol. Plant. 84, 606–615Google Scholar
  4. Bar-Noy, S., Cabantchik, Z.I. (1990) Transport domain of the erythrocyte anion exchange protein. J. Membr. Biol. 115, 217–228Google Scholar
  5. Beer, S., Israel, A. (1986) Photosynthesis of Ulva sp. III. O2 effects, carboxylase activities and the CO2 incorporation pattern. Plant Physiol. 81, 937–938Google Scholar
  6. Beer, S., Israel, A. (1990) Photosynthesis of Ulva fasciata. IV. pH, carbonic anhydrase and inorganic carbon conversions in the unstirred layer. Plant Cell Environ. 13, 555–560Google Scholar
  7. Beer, S., Israel, A., Drechsler, Z., Cohen, Y. (1990) Photosynthesis in Ulva fasciata. V. Evidence for an inorganic carbon concentrating system, and Rubisco CO2 kinetics. Plant Physiol. 94, 1542–1546Google Scholar
  8. Beer, S., Sand-Jensen, K., Vindbaek Madsen, T., Nielsen, S.L. (1991) The carboxylase activity of Rubisco and the photosynthetic performance in aquatic plants. Oecologia 87, 429–434Google Scholar
  9. Björk, M., Haglund, K., Ramazanov, Z., Garcia-Reina, G., Pedersen, M. (1992) Inorganic-carbon assimilation in the green seaweed Ulva rigida C. Ag. (Chlorophyta). Planta 187, 152–156Google Scholar
  10. Cabantchik, Z.I. (1990) The anion transport system of red blood cell membranes. In: Blood cell chemistry, pp. 337–364, Harris, M. ed., Plenum Press, New YorkGoogle Scholar
  11. Cabantchik, Z.I., Greger, R. (1992) Chemical probes for anion transporters of animal cell membranes. Am. J. Physiol. 265, C803-C827Google Scholar
  12. Cabantchik, Z.I., Rothstein, A. (1974) Membrane proteins related to anion permeability of human red blood cells. I. Localization of disulphonic stilbene binding sites in proteins involved in permeation. J. membr. Biol. 115, 207–226Google Scholar
  13. Cabantchik, Z.I., Balshin, M., Breuer, W., Rothstein, A. (1975) Pyridoxal phosphate — an anionic probe for protein amino groups exposed on the outer and inner surfaces of intact human red blood cells. J. Biol. Chem. 250, 5130–5136Google Scholar
  14. Colman, B. (1984) The effect of temperature and oxygen on the CO2 compensation point of the marine alga Ulva lactuca. Plant Cell Environ. 7, 619–621Google Scholar
  15. Cook, C.M., Lanaras, T., Colman, B. (1986) Evidence for bicarbonate transport in species of red and brown macrophytic marine algae. J. Exp. Bot. 37, 977–984Google Scholar
  16. Drechsler, Z., Beer, S. (1991) The utilization of inorganic carbon by Ulva lactuca. Plant Physiol. 97, 1439–1444Google Scholar
  17. Falke, J.J., Chan, S.I. (1986) Molecular mechanisms of band 3 inhibitors. I. Transport site inhibitors. Biochemistry. 25, 7888–7894Google Scholar
  18. Giordano, M., Maberly, S.C. (1989) Distribution of carbonic anhydrase in British marine macroalgae. Oecologia 81, 534–539Google Scholar
  19. Gutknecht, J., Bisson, M.A., Tostesson, F.C. (1977) Diffusion of carbon dioxide through lipid bilayer membranes: Effects of carbonic anhydrase, bicarbonate, and unstirred layers. J. Gen. Physiol. 69, 779–794Google Scholar
  20. Hargrave, P.A. (1986) Topography of membrane proteins-determination of regions exposed to the aqueous phase. In: Techniques for the analysis of membrane proteins, pp. 129–184m, Ragan, C.I., Cherry, R.J. eds. Chapman and Hall, LondonGoogle Scholar
  21. Jennings, M.L. (1985) Kinetics and mechanism of anion transport in red blood cells. Annu. Rev. Physiol. 47, 519–533Google Scholar
  22. Jennings, M.L. (1992) Anion transport proteins. In: The kidney: physiology and pathophysiology, 2nd edn., Seldin, D.W., Giebish, G. eds. Raven Press, New York, in pressGoogle Scholar
  23. Johnson, K.F. (1982) Carbon dioxide hydration and dehydration kinetics in seawater. Limn. Oceanogr. 27, 849–855Google Scholar
  24. Kerby, N.W., Raven, J.A. (1985) Transport and fixation of inorganic carbon by marine algae. Adv. Bot. Res. 11, 71–122Google Scholar
  25. Knauf, P.A. (1979) Erythrocyte anion exchange and the band 3 protein: Transport kinetics and molecular structure. Curr. Top. Membr. Transp. 12, 249–363Google Scholar
  26. Kopito, R.R. (1990) Molecular biology of the anion exchanger gene family. Int. Rev. Physiol. 53, 549–564Google Scholar
  27. Kremer, B. (1981) Aspects of carbon metabolism in marine macroalgae. Oceanogr. Mar. Biol. Annu. Rev. 19, 41–94Google Scholar
  28. Kuchitsu, K., Tsuzuki, M., Miyachi, S. (1991) Polypeptide composition and enzyme activities of the pyrenoid and its regulation by CO2 concentration in unicellular green algae. Can. J. Bot. 69, 1062–1069Google Scholar
  29. Lundberg, P., Weich, R.G., Jensen, P., Vogel, H.J. (1989) Phosphorus-31 and nitrogen-14 NMR studies of the uptake of phosphorus and nitrogen compounds in the marine macroalga Ulva lactuca. Plant Physiol. 89, 1380–1387Google Scholar
  30. Maberly, S.C. (1992) Carbonate ions appear to neither inhibit nor stimulate use of bicarbonate ions in photosynthesis by Ulva lactuca. Plant Cell Environ. 15, 255–260Google Scholar
  31. Nanri, H., Hamasaki, N., Minakami, S. (1983) Affinity labeling of erythrocyte band 3 protein with pyridoxal 5-phosphate. J. Biotech. Chem. 258, 5985–5989Google Scholar
  32. Passow, H. (1986) Molecular aspects of band 3 protein-mediated anion transport across red blood cell membranes. Rev. Physiol. Biochem. Pharmacol. 103, 62–217Google Scholar
  33. Price, G.D., Badger, M.R. (1991) Evidence for the role of carboxysomes in the cyanobacterial CO2-concentrating mechanism. Can. J. Bot. 69, 963–973Google Scholar
  34. Reiskind, J., Beer, S., Bowes, G. (1989) Photosynthesis and photorespiration in marine macroalgae. Aquat. Bot. 34, 131–152Google Scholar
  35. Ship, S., Shami, Y., Breuer, V.W., Rothstein, A. (1977) Synthesis of tritiated (3H)DIDS and its covalent reaction with sites related to anion transport in red blood cells. J. Membr. Biol. 33, 311–324Google Scholar
  36. Smith, R.G., Bidwell, R.G.S. (1989) Mechanisms of photosynthetic carbon dioxide uptake by the red macroalga, Chondrus crispus. Plant Physiol. 89, 93–99Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • Zivia Drechsler
    • 1
  • Rajach Sharkia
    • 1
  • Z. Ioav Cabantchik
    • 2
  • Sven Beer
    • 1
  1. 1.Department of BotanyTel Aviv UniversityTel AvivIsrael
  2. 2.Department of Biological ChemistryThe Hebrew UniversityJerusalemIsrael

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