Skip to main content
Log in

A model of carbon dioxide assimilation in Chlamydomonas reinhardii

  • Published:
Planta Aims and scope Submit manuscript

Abstract

A simple model of photosynthetic CO2 assimilation in Chlamydomonas has been developed in order to evaluate whether a CO2-concentrating system could explain the photosynthetic characteristics of this alga (high apparent affinity for CO2, low photorespiration, little O2 inhibition of photosynthesis, and low CO2 compensation concentration). Similarly, the model was developed to evaluate whether the proposed defects in the CO2-concentrating system of two Chlamydomonas mutants were consistent with their observed photosynthetic characteristics. The model treats a Chlamydomonas cell as a single compartment with two carbon inputs: passive diffusion of CO2, and active transport of HCO -3 . Internal inorganic carbon was considered to have two potential fates: assimilation to fixed carbon via ribulose 1,5-bisphosphate carboxylase-oxygenase or exiting the cell by either passive CO2 diffusion or reversal of HCO -3 transport. Published values for kinetic parameters were used where possible. The model accurately reproduced the CO2-response curves of photosynthesis for wild-type Chlamydomonas, the two mutants defective in the CO2-concentrating system, and a double mutant constructed by crossing these two mutants. The model also predicts steady-state internal inorganic-carbon concentrations in reasonable agreement with measured values in all four cases. Carbon dioxide compensation concentrations for wild-type Chlamydomonas were accurately predicted by the model and those predicted for the mutants were in qualitative agreement with measured values. The model also allowed calculation of approximate energy costs of the CO2-concentrating system. These calculations indicate that the system may be no more energy-costly than C4 photosynthesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

Chl:

chlorophyll

RuBPC/O:

ribulose 1,5-bisphosphate carboxylase-oxygenase

CA:

carbonic anhydrase

References

  • Badger, M.R., Andrews, T.J. (1982) Photosynthesis and inorganic carbon usage by the marine cyanobacterium, Synechococcus sp. Plant Physiol. 70, 517–523

    Google Scholar 

  • Badger, M.R., Kaplan, A., Barry, 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., Raven, J. (1981) Transport of inorganic carbon and the “CO2 concentrating mechanism” in Chlorella emersonii (Chlorophyceae). J. Phycol. 17, 134–141

    Google Scholar 

  • Berry, J., Boynton, J., Kaplan, A., Badger, M. (1976) Growth and photosynthesis of Chlamydomonas reinhardtii as a function of CO2 concentration. Carnegie Instn. Washington Yearb. 75, 423–432

    Google Scholar 

  • Berry, J., Farquhar, G. (1978) The CO2 concentrating function of C4 photosynthesis. A biochemical model. In: Proc. IV Int. Photosynthesis Congr., pp. 119–131, Hall, D.O., Coombs, J., Goodwin, T.W., eds. Biochemical Society, London, UK

    Google Scholar 

  • Birmingham, B.C., Colman B. (1979) Measurements of carbon dioxide compensation points of freshwater algae. Plant Physiol. 64, 892–895

    Google Scholar 

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

    Google Scholar 

  • Edwards, G.E., Huber, S.C., Ku, S.B., Rathnam, C.K.M., Gutierrez, M., Mayne, B.C. (1976) Variation in photochemical activities of C4 plants in relation to CO2 fixation. In: CO2 metabolism and productivity in plants, pp. 83–112, Black, CC., Burris, R.H., eds. University Park Press, Baltimore, MD., USA

    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. 79, 426–437

    Google Scholar 

  • Heldt, H.W. (1980) Measurement of metabolite movement across the envelope and the pH in the stroma and the thylakoid space in intact chloroplasts. Methods Enzymol. 69, 604–613

    Google Scholar 

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

    Google Scholar 

  • Jordan, D., Ogren, W.L. (1981) Species variation in the specificity of ribulose bisphosphate carboxlase/oxygenase. Nature 291, 513–515

    Google Scholar 

  • Kaplan, A., Badger, M.R., Berry, J.A. (1980) Photosynthesis and the intracellular inorganic carbon pool in the blue-green alga Anabaena variabilis: response to external CO2 concentration. Planta 149, 219–226

    Google Scholar 

  • Kimpel, D.L., Togasaki, R.K., Miyachi, S. (1983) Carbonic anhydrase in Chlamydomonas reinhardtii. I. Localization. Plant Cell Physiol. 24, 255–259

    Google Scholar 

  • Laing, W.A., Ogren, W.L., Hageman, R.H. (1974) Regulation of soybean net photosynthetic CO2 fixation by the interaction of CO2, O2 and ribulose 1,5-diphosphate carboxylase. Plant Physiol. 54, 678–685

    Google Scholar 

  • Lloyd, N.D., Canvin, D.T., Culver, D.A. (1977) Photosynthesis and photorespiration in algae. Plant Physiol. 59, 936–940

    Google Scholar 

  • Nilsen, S., Johnsen, O. (1982) Effect of CO2, O2 and diamox on photosynthesis and photorespiration in Chlamydomonas reinhardtii (green alga) and Anacystis nidulans (cyanobacterium, blue-green alga). Physiol. Plant. 56, 273–280

    Google Scholar 

  • Nobel, P.S. (1974) Biophysical plant physiology. W.H. Freeman & Co., San Francisco

    Google Scholar 

  • Ogawa, T., Inoue, Y., Lilley, R. McC., Ogren, W.L. (1984) A post-illumination CO2 burst in Anabaena variabilis as a measure of bicarbonate transport driven by cyclic photophosphorylation. In: Advances in photosynthesis research, vol. II, pp. 723–726, Sybesma, C., ed. Nijhoff/Junk, The Hague

    Google Scholar 

  • Pocker, Y., Bjorkquist, D.W. (1977) Stopped flow studies of carbon dioxide hydration and bicarbonate dehydration in H2O and D2O. Acid-base and metal ion catalysis. J. Am. Chem. Soc. 99, 6537–6543

    Google Scholar 

  • Pocker, Y., Miksch, R.R. (1978) Plant carbonic anhydrase. Properties and bicarbonate dehydration kinetics. Biochemistry 17, 1119–1125

    Google Scholar 

  • Pocker, Y., Ng, J.S.Y. (1973) Plant carbonic anhydrase. Properties and carbon dioxide hydration kinetics. Biochemistry 12, 5127–5134

    Google Scholar 

  • Savageau, M.A. (1976) Biochemical systems analysis. Addison-Wesley Pub. Co., Reading, Mass.

    Google Scholar 

  • Silverman, D.N., Tu, C., Wynns, G.C. (1976) Depletion of 18O from C18O2 in erythrocyte suspensions. The permeability of the erythrocyte membrane to CO2. J. Biol. Chem. 251, 4428–4435

    Google Scholar 

  • Sirs, J.A. (1958) Electronmetric stopped-flow measurements of rapid reactions in solution. 2. Glass electrode pH measurements. Trans. Faraday Soc. 54, 207–212

    Google Scholar 

  • Spalding, M.H., Ogren, W.L. (1982) Photosynthesis is required for induction of the CO2-concentrating system in Chlamydomonas reinhardii. FEBS Lett. 145, 41–44

    Google Scholar 

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

    Google Scholar 

  • Spalding, M.H., Ogren, W.L. (1985) CO2 exchange characteristics during dark to light transitions in wild type and mutant Chlamydomonas reinhardii cells. Photosynth. Res. (in press)

  • Spalding, M.H., Spreitzer, R.J., Ogren, W.L. (1983a) Carbonic anhydrase deficient mutant of Chlamydomonas requires elevated carbon dioxide concentration for photoautotrophic growth. Plant Physiol. 73, 268–272

    Google Scholar 

  • Spalding, M.H., Spreitzer, R.J., Ogren, W.L. (1983b) Reduced inorganic carbon transport in a CO2-requiring mutant of Chlamydomonas reinhardii. Plant Physiol. 73, 273–276

    Google Scholar 

  • Spalding, M.H., Spreitzer, R.J., Ogren, W.L. (1983c) Genetic and physiological analysis of the CO2-concentrating system of Chlamydomonas reinhardii. Planta 159, 261–266

    Google Scholar 

  • Spalding, M.H., Spreitzer, R.J., Ogren, W.L. (1985) Use of mutants in analysis of the CO2-concentrating pathway of Chlamydomonas reinhardii. In: Inorganic carbon uptake by photosynthetic organismus, Lucas, W., Berry, J., eds. American Society of Plant Physiologists. Rockville, Md., USA

    Google Scholar 

  • Spalding, M.H., Stumpf, D.K., Ku, M.S.B., Burris, R.H., Edwards, G.E. (1979) Crassulacean acid metabolism and diurnal variations of internal CO2 and O2 concentration in Sedum praealtum DC. Aust. J. Plant Physiol. 6, 557–567

    Google Scholar 

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

    Google Scholar 

  • Umbreit, W.E., Burris, R.H., Stauffer, J.F. (1945) Manometric techniques and related methods for the study of tissue metabolism. Burgess Publishing Co., Minneapolis

    Google Scholar 

  • Wintermans, J.F.G.M., De Mots, A. (1965) Spectrophotometric characteristics of chlorophyll and their pheophytins in ethanol. Biochim. Biophys. Acta 109, 448–453

    Google Scholar 

  • Wissburn, K.F., French, R.M., Patterson, A. (1954) The true ionization constant of carbonic acid in aqueous solution from 5° to 45°. J. Phys. Chem. 58, 693–695

    Google Scholar 

  • Zenvirth, D., Kaplan, A. (1981) Uptake and efflux of inorganic carbon in Dunaliella salina. Planta 152, 8–12

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Spalding, M.H., Portis, A.R. A model of carbon dioxide assimilation in Chlamydomonas reinhardii . Planta 164, 308–320 (1985). https://doi.org/10.1007/BF00402942

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00402942

Key words

Navigation