, Volume 187, Issue 2, pp 275–281 | Cite as

Role of carbonic anhydrase in photosynthesis and inorganic-carbon assimilation in the red alga Gracilaria tenuistipitata

  • Kurt Haglund
  • Mats Björk
  • Ziyadin Ramazanov
  • Guillermo García-Reina
  • Marianne Pedersén


The mechanism of inorganic-carbon (Ci) accumulation in the red seaweed Gracilaria tenuistipitata Zhang et Xia has been investigated. Extracellular and intracellular carbonic-anhydrase (CA) activities have been detected. Photosynthetic O2 evolution in thalli and protoplasts of G. tenuistipitata were higher at pH 6.5 than at pH 8.6, where HCO3is the predominant form of Ci. Dextran-bound sulfonamide (DBS), a specific inhibitor of extracellular CA, reduced photosynthetic O2 evolution at pH 8.6 and did not have any effect at pH 6.5. After inhibition with DBS, O2 evolution was similar to the rate that could be supported by CO2 from spontaneous dehydration of HCO3. The rate of photosynthetic alkalization of the surrounding medium by the algal thallus was dependent on the concentration of Ci and inhibited by DBS. We suggest that the general form of Ci that enters through the plasma membrane of G. tenuistipitata is CO2. Bicarbonate is utilized mainly by an indirect mechanism after dehydration to CO2, and this mechanism involves extracellular CA.

Key words

Carbon assimilation Carbonic anhydrase Carbon dioxide uptake Gracilaria Photosynthesis 



inorganic carbon (CO2 + HCO3)


carbonic anhydrase


dissolved inorganic carbon (total)


dextran-bound sulfonamide




natural seawater


photosynthetic photon flux density


relative enzyme activity


ribulose-1,5-bisphosphate carboxylase/oxygenase


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  1. Axelsson, L. (1988) Changes in pH as a measure of photosynthesis by marine macroalgae. Mar. Biol. 97, 287–294Google Scholar
  2. Beardall, J. (1981) CO2 accumulation by Chlorella saccharophila (Chlorophyceae) at low external pH: evidence for active transport of inorganic carbon at the chloroplast envelope. J. Phycol. 17, 371–373Google Scholar
  3. 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, 555–60Google Scholar
  4. Beer, S., Israel, A., Drechsler, Z., Cohen, Y. (1990) Photosynthesis in Ulva fasciata V. Evidence for an inorganic carbon concentrating system, and ribulose-1,5-bisphosphate carboxylase/ oxygenase CO2 kinetics. Plant Physiol. 94, 1542–1546Google Scholar
  5. Bidwell, R.G.S., McLachlan, J. (1985) Carbon nutrition of seaweeds: photosynthesis, photorespiration and respiration. J. Exp. Mar. Biol. Ecol. 86, 15–46Google Scholar
  6. Björk, M., Ekman, P., Wallin, A., Pedersén, M. (1990) Effects of growth rate and other factors on protoplast yield from four species of the red seaweed Gracilaria (Rhodophyta). Bot. Mar. 33, 433–439Google Scholar
  7. Björk, M., Haglund, K., Ramazanov, Z., García-Reina, G., Pedersén, M. (1992) Inorganic carbon assimilation in the green seaweed Ulva rigida (Chlorophyta). Planta 187, 152–156Google Scholar
  8. Bowes, G.W. (1969) Carbonic anhydrase in marine algae. Plant Physiol. 44, 726–732Google Scholar
  9. Bréchignac, F., André, M., Gerbaud, A. (1986) Preferential photosynthetic uptake of exogenous HCO3 in the marine macroalga Chondrus crispus. Plant Physiol. 80, 1059–1062Google Scholar
  10. Burns, B.D., Beardall, J. (1988) Utilization of inorganic carbon by marine microalgae. J. Exp. Mar. Biol. Ecol. 107, 75–86Google Scholar
  11. Coleman, J.R., Rotatore, C., Williams, T.G., Colman, B. (1991) Identification and localization of carbonic anhydrase in two Chlorella species. Plant Physiol. 95, 331–334Google Scholar
  12. 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
  13. Cook, C.M., Lanaras, T., Roubelakis-Angelakis, K.A. (1988) Bicarbonate transport and alkalization of the medium by four species of Rhodophyta. J. Exp. Bot. 39, 1185–1198Google Scholar
  14. Enns, T. (1967) Facilitation by carbonic anhydrase of carbon dioxide transport. Science 155, 44–47Google Scholar
  15. Giordano, M., Maberly, S.C. (1989) Distribution of carbonic anhydrase in British marine macroalgae. Oecologia 81, 534–539Google Scholar
  16. Graham, D., Smillie, R.M. (1976) Carbonate dehydratase in marine organisms of the Great Barrier Reef. Aust. J. Plant Physiol. 3, 113–119Google Scholar
  17. Gutknecht, J., Bisson, M.A., Tosteson, 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
  18. Haglund, K., Axelsson, L., Pedersén, M. (1987) Photosynthesis and respiration in the alga Ahnfeltia plicata in a flow-through system. Mar. Biol. 96, 409–412Google Scholar
  19. Johnson, K.S. (1982) Carbon dioxide hydration and dehydration kinetics in seawater. Limnol. Oceanogr. 27, 849–855Google Scholar
  20. Jolliffe, E.A., Tregunna, E.B. (1970) Studies on HCO3 ion uptake during photosynthesis in benthic marine algae. Phycologia 9, 293–303Google Scholar
  21. Kerby, N.W., Raven, J.A. (1985) Transport and fixation of inorganic carbon by marine algae. Adv. Bot. Res. 11, 71–123Google Scholar
  22. Lindahl, P.E.B. (1963) The inhibition of the photosynthesis of aquatic plants by tetramethylthiuram disulphide. Symbolae Bot. Upsalienses 17, 1–47Google Scholar
  23. Lignell, Å., Ekman, P., Pedersén, M. (1987) Cultivation technique for marine seaweeds allowing controlled and optimized conditions in the laboratory and on a pilotscale. Bot. Mar. 30, 417–424Google Scholar
  24. Lignell, Å., Pedersén, M. (1989) Effects of pH and inorganic carbon concentrations on growth of Gracilaria secundata. Br. Phycol. J. 24, 83–89Google Scholar
  25. Lucas, W.J. (1983) Photosynthetic assimilation of exogenous HCO3 by aquatic plants. Annu. Rev. Plant Physiol. 34, 71–104Google Scholar
  26. Maberly, S.C. (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J. Phycol. 26, 439–449Google Scholar
  27. Moroney, J.V., Husic, D.H., Tolbert, N.E. (1985) Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol. 77, 177–183Google Scholar
  28. Moroney, J.V., Kitayama, M., Tokasaki, R.K., Tolbert, N.E. (1987) Evidence for inorganic carbon transport by intact chloroplasts of Chlamydomonas reinhardtii. Plant Physiol. 83, 460–463Google Scholar
  29. Palmqvist, K., Ramazanov, Z., Samuelsson, G. (1990a) The role of extracellular carbonic anhydrase for accumulation of inorganic carbon in the green alga Chlamydomonas reinhardtii. A comparison between wild-type and cell-wall-less mutant cells. Physiol. Plant. 80, 267–276Google Scholar
  30. Palmqvist, K., Ramazanov, Z., Gardeström, P., Samuelsson, G. (1990b) Adaption mechanisms in microalgae to conditions of carbon dioxide-limited photosynthesis. Possible role of carbonic anhydrase. Fiziol. Rast. (Moscow) 37, 912–920Google Scholar
  31. Peterson, G.L. (1983) Determination of total protein. Methods Enzymol. 91, 95–119Google Scholar
  32. Provasoli, L. (1968) Media and prospects for the cultivation of marine algae. In: Cultures and Collections of Algae (Proc. US-Japan Conf., Hakone), pp. 63–75, Watanabe, A., Hattori, A., eds. Jpn. Soc. Plant Physiol.Google Scholar
  33. Ramazanov, Z.M., Semenenko, V.E. (1988) Content of the CO2-dependent form of carbonic anhydrase as a function of light intensity and photosynthesis. Sov. Plant Physiol. 35, 340–344Google Scholar
  34. Raven, J.A., Lucas, W.J. (1985) The energetics of carbon acquisition. In: Inorganic carbon uptake by aquatic photosynthetic organisms, pp. 305–324, Lucas, W.J., Berry, J.A., eds. American Society of Plant Physiologists. Rockwell, MarylandGoogle Scholar
  35. Reiskind, J.B., Seamon, P.T., Bowes, G. (1988) Alternative methods of photosynthetic carbon assimilation in marine macroalgae. Plant Physiol. 87, 686–692Google Scholar
  36. Sand-Jensen, K., Gordon, D.M. (1984) Differential ability of marine and freshwater macrophytes to utilize HCO3 and CO2. Mar. Biol. 80, 247–253Google Scholar
  37. Skirrow, G. (1975) The dissolved gases — carbon dioxide. In: Chemical oceanography, vol. 2, pp. 1–192, Riley, J.P., Skirrow, G., eds. Academic Press, London New York San FranciscoGoogle Scholar
  38. Smith, R.G., Bidwell, R.G.S. (1987) Carbonic anhydrase-dependent inorganic carbon uptake by the red macroalga, Chondrus crispus. Plant Physiol. 83, 735–738Google Scholar
  39. Smith, R.G., Bidwell, R.G.S. (1989a) Mechanism of photosynthetic carbon dioxide uptake by the red macroalga, Chondrus crispus. Plant Physiol. 89, 93–99Google Scholar
  40. Smith, R.G., Bidwell, R.G.S. (1989b) Inorganic carbon uptake by photosynthetically active protoplasts of the red macroalga Chondrus crispus. Mar. Biol. 102, 1–44Google Scholar
  41. Sültemeyer, D.F., Miller, A.G., Espie, G.S., Fock, H.P., Canvin, D.T. (1989) Active CO2 transport by the green alga Chlamydomonas reinhardtii. Plant Physiol. 89, 1213–1219Google Scholar
  42. Sültemeyer, D.F., Fock, H.P., Canvin, D.T. (1990) Mass spectrometric measurement of intracellular carbonic anhydrase activity in high and low Ci cells of Chlamydomonas. Studies using 18O exchange with 13C/18O labeled bicarbonate. Plant Physiol. 94, 1250–1257Google Scholar
  43. Surif, M.B., Raven, J.A. (1989) Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and Laminariales (Phaeophyta): ecological and taxonomic implications. Oecologia 78, 97–105Google Scholar
  44. Tinker, J.P., Coulson, R., Weiner, I.M. (1981) Dextran-bound inhibitors of carbonic anhydrase. J. Pharmacol. Exp. Ther. 218, 600–607Google Scholar
  45. Tseng, C.K., Sweeney, B.M. (1946) Physiological studies of Gelidium cartilagineum. I. Photosynthesis, with special reference to the carbon dioxide factor. Am. J. Bot. 33, 706–715Google Scholar
  46. Wintermans, J.F.G., De Mots, A. (1965) Spectrophotometric characteristics of chlorophylls a and b and their pheophytins in ethanol. Biochim. Biophys. Acta 109, 448–453Google Scholar
  47. Yagawa, Y., Muto, S., Miyachi, S. (1987) Carbonic anhydrase of a unicellular red alga Porphyridium cruentum R-1. II. Distribution and role in photosynthesis. Plant Cell Physiol. 28, 1509–1516Google Scholar

Copyright information

© Springer-Verlag 1992

Authors and Affiliations

  • Kurt Haglund
    • 1
  • Mats Björk
    • 1
  • Ziyadin Ramazanov
    • 2
  • Guillermo García-Reina
    • 3
  • Marianne Pedersén
    • 1
  1. 1.Department of Physiological BotanyUppsala UniversityUppsalaSweden
  2. 2.Institute of Plant Physiology, Russian Academy of SciencesMoscowRussian Federation
  3. 3.Marine Plant Biotechnology Laboratory, University of Las PalmasLas PalmasSpain

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