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Role of intracellular carbonic anhydrase in inorganic-carbon assimilation by Porphyridium purpureum

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Abstract

Air-grown cells of Porphyridium purpurem contain appreciable carbonic-anhydrase activity, comparable to that in air-grown Chlamydomonas reinhardtii, but activity is repressed in CO2-grown cells. Assay of carbonic-anhydrase activity in intact cells and cell extracts shows all activity to be intracellular in Porphyridium. Measurement of inorganic-carbon-dependent photosynthetic O2 evolution shows that sodium ions increase the affinity of Porphyridium cells for HCO -3 . Acetazolamide and ethoxyzolamide were potent inhibitors of carbonic anhydrase in cell extracts but at pH 5.0 both acetazolamide and ethoxyzolamide had little effect upon the concentration of inorganic carbon required for the half-maximal rate of photosynthetic O2 evolution (K0.5[CO2]). At pH 8.0, where HCO -3 is the predominant species of inorganic carbon, the K0.5 (CO2) was increased from 50 μM to 950 μM in the presence of ethoxyzolamide. It is concluded that in air-grown cells of Porphyridium. HCO -3 is transported across the plasmalemma and intracellular carbonic anhydrase increases the steady-state flux of CO2 from inside the plasmalemma to ribulose-1,5-bisphosphate carboxylase-oxygenase by catalysing the interconversion of HCO -3 and CO2 within the cell.

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Abbreviations

AZ:

acetazolamide

EZ:

ethoxyzolamide

K0.5[CO2]:

half-maximal rate of photosynthetic O2 evolution

References

  • Badger, M.R., Kaplan, A., Berry, J.A. (1980) Internal inorganic carbon pool of Chlamydomonas reinhardtii. Evidence for a carbon dioxide concentrating mechanism. Plant Physiol. 66, 407–413

    Google Scholar 

  • Beardall, J. (1981) CO2 accumulation by Chlorella saccharophilia (Chlorophyceae) at low external pH. J. Phycol. 17, 371–373

    Google Scholar 

  • Beardall, J., Morris, I. (1975) Effect of environmental factors on photosynthetic patterns in Phaeodactylum tricornutum (Bacillariophyceae) II. Effect of oxygen. J. Phycol. 2, 430–434

    Google Scholar 

  • Beardall, J., Raven, J.A. (1981) Transport of inorganic carbon and the CO2 concentrating mechanism in Chlorella emersonii (Chlorophyceae). J. Phycol. 17, 134–141

    Google Scholar 

  • Bundy, H.F., Cote, S. (1980) Purification and properties of carbonic anhydrase from Chlamydomonas reinhardtii. Phytochemistry 19, 2531–2534

    Google Scholar 

  • Coleman, J.R., Berry, J.A., Togasaki, R.K., Grossman, R.A. (1984) Identification of extracellular carbonic anhydrase of Chlamydomonas reinhardtii. Plant Physiol. 76, 472–477

    Google Scholar 

  • Coleman, J.R., Colman, B. (1981) Inorganic carbon accumulation and photosynthesis in a blue-green alga as a function of pH. Plant Physiol. 67, 917–921

    Google Scholar 

  • Colman, B., Gehl, K.A. (1983) Physiological characteristics of photosynthesis in Porphyridium cruentum: evidence for bicarbonate transport in a unicellular red alga. J. Phycol. 19, 216–219

    Google Scholar 

  • Cook, C.M., Lanoras, T., Colman, B. (1966) Evidence for bicarbonate transport in species of red and brown macrophytic marine algae. J. Exp. Bot. 37, 977–984

    Google Scholar 

  • Findenegg, G.R. (1976) Correlations between accessibility of carbonic anhydrase for external substrate and regulation of photosynthetic use of CO2 and HCO -3 by Scenedesmus obliquus. Z. Pflanzenphysiol. 89, 363–371

    Google Scholar 

  • Hartree, E.F. (1972) A modification of the Lowry method that gives a linear photometric response. Anal. Biochem. 48, 422–427

    Google Scholar 

  • Hogetsu, D., Miyachi, S. (1977) Effects of CO2 concentration during growth on subsequent photosynthetic CO2 fixation in Chlorella. Plant Cell Physiol. 18, 347–352

    Google Scholar 

  • Imamura, M., Tsuzuki, M., Shiraiwa, Y., Miyachi, S. (1983) Form of inorganic carbon utilized for photosynthesis in Chlamydomonas reinhardtii. Plant Cell Physiol. 24, 533–540

    Google Scholar 

  • Kaplan, A., Volokita, M., Zenvirth, D., Reinhold, L. (1984) An essential role for sodium in the bicarbonate transporting system of the cyanobacterium Anabaena variablis. FEBS Lett. 176, 166–168

    Google Scholar 

  • 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 cyanobacterium Anabaena variablis. Plant Physiol. 69, 978–982

    Google Scholar 

  • Katz, A., Kaback, H.R., Avron, M. (1986) Na+/H+ antiport in isolated plasma membrane vesicles from the halotolerant alga. Dunaliella salina. FEBS. Lett. 202, 141–144

    Google Scholar 

  • Kimpel, D.L., Togasaki, R.K., Miyachi, S. (1983) Carbonic anhydrase in Chlamydomonas reinhardtii. 1. Localization. Plant Cell Physiol. 24, 225–229

    Google Scholar 

  • Lee, R.E. (1980) Phycology. pp. 478, Cambridge University Press, London and New York

    Google Scholar 

  • Maren, T.H. (1984) The general physiology of reactions catalyzed by carbonic anhydrase and their inhibition by sulfonamides. Ann. N.Y. Acad. Sci. 429, 568–579

    Google Scholar 

  • Miller, A.G., Canvin, D.T. (1985) Distinction between HCO -3 and CO2-dependent photosynthesis in the cyanobacterium Synechococcus leopoliensis based on the selective response of HCO -3 transport to Na+. FEBS Lett. 187, 29–32

    Google Scholar 

  • Moroney, J.V., Husic, H.D., Tolbert, N.E. (1985) Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol. 79, 177–183

    Google Scholar 

  • Moroney, J.V., Tolbert, N.E. (1985) Inorganic carbon uptake by Chlamydomonas reinhardtii. Plant Physiol. 77, 253–258

    Google Scholar 

  • Nelson, E.R., Cenedella, A., Tolbert, N.E. (1969) Carbonic anhydrase levels in Chlamydomonas. Phytochemistry 8, 2305–2306

    Google Scholar 

  • Patel, B.N., Merrett, M.J. (1986a) Regulation of carbonic-anhydrase activity, inorganic-carbon uptake and photosynthetic biomass yield in Chlamydomonas reinhardtii. Planta 169, 81–86

    Google Scholar 

  • Patel, B.N., Merrett, M.J. (1986b) Inorganic-carbon uptake by the marine diatom Phaeodactylum ticornutum. Planta 169, 222–227

    Google Scholar 

  • Provasoli, L., McLaughlin, J.J.A., Droop, M.R. (1957) The development of arifical media for marine algae. Arch. Mikrobiol. 25, 392–428

    Google Scholar 

  • Rees, T.A.V. (1984) Sodium dependent photosynthetic oxygen evolution in a marine diatom. J. Exp. Bot. 35, 332–337

    Google Scholar 

  • Shelp, B.J., Canvin, D.T. (1985) Inorganic carbon accumulation and photosynthesis by Chlorella pyrenoidosa. Can. J. Bot. 63, 1249–1254

    Google Scholar 

  • Spalding, M.H., Ogren, W.L. (1983) Evidence for a saturable transport component in the inorganic carbon uptake of Chlamydomonas reinhardtii. FEBS Lett. 154, 335–338

    Google Scholar 

  • Tsuzuki, M. (1983) Mode of HCO -3 utilization by the cells of Chamydomonas grown under ordinary air. Z. Pflanzenphysiol. 110, 29–37

    Google Scholar 

  • Wilbur, K.M., Anderson, N.G. (1948) Electrometric and colorimetric determination of carbonic anhydrase. J. Biol. Chem. 176, 147–154

    Google Scholar 

  • Woolf, B. (1932) Quoted in J.B.S. Haldane and K.G. Stern. Allgemeine Chemie der Enzyme, p. 119, Steinkopff-Verlag, Dresden and Leipzig

    Google Scholar 

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Authors and Affiliations

  1. Plant and Microbial Metabolism Research Group, School of Biological Sciences, University College of Swansea, Singleton Park, SA2 8PP, Swansea, UK

    G. K. Dixon, B. N. Patel & M. J. Merrett

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  1. G. K. Dixon
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  2. B. N. Patel
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  3. M. J. Merrett
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Dixon, G.K., Patel, B.N. & Merrett, M.J. Role of intracellular carbonic anhydrase in inorganic-carbon assimilation by Porphyridium purpureum . Planta 172, 508–513 (1987). https://doi.org/10.1007/BF00393867

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  • DOI: https://doi.org/10.1007/BF00393867

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