Abstract
The regulation of carbonic anhydrase by environmental conditions was determined forChlamydomonas reinhardtii. The depression of carbonic anhydrase in air-grown cells was pH-dependent. Growth of cells on air at acid pH, corresponding to 10 μm CO2 in solution, resulted in complete repression of carbonic-anhydrase activity. At pH 6.9, increasing the CO2 concentration to 0.15% (v/v) in the gas phase, corresponding to 11 μM in solution, was sufficient to completely repress carbonic-anhydrase activity. Photosynthesis and intracellular inorganic carbon were measured in air-grown and high-CO2-grown cells using a silicone-oil centrifugation technique. With carbonic anhydrase repressed cells limited inorganic-carbon accumulation resulted from non-specific binding of CO2. With air-grown cells, inorganic-carbon uptake at acid pH, i.e. 5.5, was linear up to 0.5 mM external inorganic-carbon concentration whereas at alkaline pH, i.e. 7.5, the accumulation ratio decreased with increase in external inorganic-carbon concentration. It is suggested that in air-grown cells at acid pH, CO2 is the inorganic carbon species that crosses the plasmalemma. The conversion of CO2 to HCO -3 by carbonic anhydrase in the cytosol results in inorganic-carbon accumulation and maintains the diffusion gradient for carbon dioxide across the cell boundary. However, this mechanism will not account for energy-dependent accumulation of inorganic carbon when there is little difference in pH between the exterior and cytosol.
Similar content being viewed by others
References
Badger, M.R., Kaplan, A., Berry, J.A. (1980) Internal inorganic carbon pool ofChlamydomonas reinhardtii. Evidence for a carbon-dioxide concentrating mechanism. Plant Physiol.66, 407–413
Beardall, J. (1981) CO2 accumulation byChlorella saccharophilia (Chlorophyceae) at low external pH. Evidence for active transport of inorganic carbon at the chloroplast envelope. J. Phycol.17, 371–373
Beardall, J., Raven, J.A. (1981) Transport of inorganic carbon and the “CO2 concentrating mechanism” inChlorella emersonii (Chlorophyceae). J. Phycol.17, 134–141
Codd, G.A., Lord, J.M., Merrett, M.J. (1969) The glycolate oxidising enzyme of algae. FEBS Lett.5, 341–342
Coleman, J.R., Coleman, B. (1981) Inorganic carbon accumulation and photosynthesis in a blue-green alga as a function of external pH. Plant Physiol.67, 917–921
Coleman, J.R., Berry, J.A., Togasaki, R.K., Grossman, R.A. (1984) Identification of extracellular carbonic anhydrase ofChlamydomonas reinhardtii. Plant Physiol.76, 472–477
Findenegg, G.R. (1976) Correlations between the accessibility of carbonic anhydrase for external substrate and regulation of photosynthetic use of CO2 and HCO -3 byScenedesmus obliquus. Z. Pflanzenphysiol.79, 428–437
Hartree, E.F. (1972) A modification of the Lowry method that gives a linear photometric response. Anal. Biochem.48, 422–427
Hogetsu, D., Miyachi, S. (1979) Role of carbonic anhydrase in photosynthetic CO2 fixation inChlorella. Plant Cell Physiol.20, 747–756
Kaplan, A., Zenvirth, D.L., Reinhold, L., Berry, J.A. (1982) Involvement of a primary electrogenic pump in the mechanism for HCO -3 uptake by the cyanobacteriumAnabaena variabilis. Plant Physiol.69, 978–982
Kimpel, D.L., Togasaki, R.K., Miyachi, S. (1983) Carbonic anhydrase inChlamydomonas reinhardtii. I. Localization. Plant Cell Physiol.24, 255–259
Marcus, Y., Volokita, M., Kaplan, A. (1984) The location of the transporting system for inorganic carbon and the nature of the form translocated inChlamydomonas reinhardtii. J. Exp. Bot.35, 1136–1144
Merrett, M.J., Armitage, T.L. (1982) The effect of oxygen concentration on photosynthetic biomass production by algae. Planta155, 95–96
Moroney, J.V., Tolbert, N.E. (1985) Inorganic carbon uptake byChlamydomonas reinhardtii. Plant Physiol.77, 253–258
Moroney, J.V., Husic, H.D., Tolbert, N.E. (1985) Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation byChlamydomonas reinhardtii. Plant Physiol.79, 177–183
Nelson, E.R., Cenedella, A., Tolbert, N.E. (1969) Carbonic anhydrase levels inChlamydomonas. Phytochemistry8, 2305–2306
Raven, J.A. (1980) Nutrient transport in microalgae. Adv. Microb. Physiol.21, 47–226
Shelp, B.J., Canvin, D.T. (1985) Thorganic carbon accumulation and photosynthesis byChlorella pyrenoidosa. Can. J. Bot.63, 1249–1254
Spalding, M.H., Ogren, W.L. (1982) Photosynthesis is required for induction of the Co2-concentrating system inChlamydomonas reinhardtii. FEBS Lett.145, 41–44
Spalding, M.H., Ogren, W.L. (1983) Evidence for a saturable transport component in the inorganic carbon uptake ofChlamydomonas reinhardtii. FEBS Lett.154, 335–338
Spalding, M.H., Spreitzer, R.J., Ogren, W.L. (1983) Reduced inorganic carbon transport in a CO2-requiring mutant ofChlamydomonas reinhardtii. Plant Physiol.73, 273–276
Wilbur, K.M., Anderson, N.G. (1948) Electrometric and colorimetric determination of carbonic anhydrase. J. Biol. Chem.176, 147–154
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Patel, B.N., Merrett, M.J. Regulation of carbonic-anhydrase activity, inorganic-carbon uptake and photosynthetic biomass yield inChlamydomonas reinhardtii . Planta 169, 81–86 (1986). https://doi.org/10.1007/BF01369778
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01369778