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Effect of vanadate on photosynthesis and the ATP/ADP ratio in low-CO2-adapted Chlamydomonas reinhardtii cells

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Abstract

We have assessed the effect of vanadate as an inhibitor of plasma-membrane ATPase on photosynthesis and the ATP/ADP ratio in Chlamydomonas reinhardtii CW-92 (a mutant strain lacking a cell wall). This effect was compared in low-CO2-adapted cells grown in media bubbled with air containing 400 or 70 μL · L−1 CO2. Evidence is presented indicating that cells grown at 70 μL · L−1 CO2 have a higher rate of photosynthetic O2 evolution than cells grown at 400 μL · L−1 CO2, at limiting carbon concentrations. Extracellular and intracellular carbonic-anhydrase activities were, however, similar in cells grown in both of the low-carbon conditions. Vanadate inhibited, to a different extent, the HCO 3 -dependent O2 evolution in cells grown at 400 and 70 μL · L−1 CO2. At 400 μM vanadate, inhibition reached 70–75% in cells grown at 400 μL · L−1 but only 50% in those grown at 70 μL · L−1 CO2. The ATP/ADP ratios determined with and without vanadate at limiting concentrations of dissolved inorganic carbon indicated that more ATP was hydrolysed in algae grown at 70 μL · L−1 than in those grown at 400 μL · L−1 CO2. We conclude that the maximal capacity to accumulate dissolved inorganic carbon is inversely related to the CO2 concentration in the medium. Activation and — or synthesis of vanadate-sensitive ATPase may be the major explanation for the higher capacity for HCO 3 -dependent O2 evolution in cells grown under limited CO2 concentrations.

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Abbreviations

CA:

carbonic anhydrase

DIC:

dissolved inorganic carbon

References

  • Aizawa, K., Miyachi, S. (1984) Carbonic anhydrase located on cell surface increases the affinity for inorganic carbon in photosynthesis of Dunaliella tertiolecta. FEBS Lett. 173, 41–44

    Google Scholar 

  • Badger, M.R. (1987) The CO2 concentrating mechanism in aquatic phototrophs. In: The biochemistry of plants. A comprehensive treatise, vol. 10, pp. 219–274, Hatch, M.D., Broaman, N.K., eds. Academic Press, San Diego, USA

    Google Scholar 

  • Badger, M.R., Kaplan, A., Berry, J.R. (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 saccharophila (Chlorophyceae) at low external pH: evidence for the active transport of inorganic carbon at the chloroplast envelope. J. Phycol. 17, 371–373

    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 

  • Bedu, S., Peltier, G., Josef, F. (1989) Correlation between carbonic anhydrase activity and inorganic carbon pool in strain Synechocystis PCC 6174. Plant Physiol. 90, 470–474

    Google Scholar 

  • Bedu, S., Peltier, G., Sarrey, F., Josef F. (1990) Properties of a mutant from Synechocystis PCC 6803 resistant to acetazolamide, an inhibitor of carbonic anhydrase. Plant Physiol. 93, 1312–1315

    Google Scholar 

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

    Google Scholar 

  • Burnell, J.N. (1990) Immunological study of carbonic anhydrase in C3 and C4 plants using antibodies to maize cytosolic and spinach chloroplastic carbonic anhydrase. Plant Cell Physiol. 31, 423–427

    Google Scholar 

  • Coleman, J.R., Grossman, A.R. (1984) Biosynthesis of carbonic anhydrase in Chlamydomonas reinhardtii during adaptation to low CO2. Proc. Natl. Acad. Sci. USA 81, 6049–6053

    Google Scholar 

  • Coleman, J.R., Rotathore, C., Williams, T.G., Colman, B. (1991) Identification and localization of carbonic anhydrase in two Chlorella species. Plant Physiol. 95, 331–334

    Google Scholar 

  • Findenegg, G.R. (1976) Correlation between accessibility of carbonic anhydrase for external substrate and regulation of photosynthetic use of CO2 and HCO 3 by Scenedesmus obliguus. Z. Pflanzenphysiol. 79, 428–437

    Google Scholar 

  • Gardeström, P., Wigge, B. (1988) The influence of photorespiration on ATP/ADP ratios in the chloroplasts, mitochondria and cytosol studied by rapid fractionation of barley (Hordeum vulgare) protoplasts. Plant-Physiol. 88. 69–78

    Google Scholar 

  • Geraghty, A.M., Anderson, J.C., Spalding, M.H. (1990) A 36 kilodalton limiting CO2 induced polypeptide of Chlamydomonas is distinct from 37 kilodalton periplasmic carbonic anhydrase. Plant Physiol. 93, 116–121

    Google Scholar 

  • Goldschmidt-Clermont, M., Malnoe, P., Rochaix, J.-D. (1989) Preparation of Chlamydomonas chloroplasts for the in vitro import of polypeptide precursors. Plant Physiol. 89, 15–18

    Google Scholar 

  • Goyal, A., Tolbert, N.E. (1989) Uptake of inorganic carbon by isolated chloroplasts from air-adapted Dunaliella. Plant Physiol. 89, 1264–1269

    Google Scholar 

  • Husic, H.D., Kitayama, M., Togasaki, R.K., Moroney, J.V., Morris, K.L., Tolbert N.E. (1989) Identification of intracellular carbonic anhydrase in Chlamydomonas reinhardtii which is distinct from the periplasmic form of the enzyme. Plant Physiol. 89, 904–909

    Google Scholar 

  • Husic, H.D., Quigley, E.A. (1990) Salt-induced dissociation of carbonic anhydrase from intact cells of Chlamydomonas reinhardtii. Plant Physiol. 94, 380–384

    Google Scholar 

  • MacKinney, G. (1941) Absorbtion of light by chlorophyll solutions. J Biol. Chem. 140, 315–322

    Google Scholar 

  • Marcus, Y., Volokita, M., Kaplan, A. (1984) The location of the transporting system for inorganic carbon and the nature of the form translocated in Chlamydomonas reinhardtii. J. Exp. Bot. 35, 1136–1144

    Google Scholar 

  • Mason, C.B., Manuel, L.J., Moroney, J.V. (1990) A new chloroplast protein is induced by growth on low CO2 in Chlamydomonas reinhardtii. Plant Physiol. 93, 833–836

    Google Scholar 

  • Moroney, J.V., Mason, C.B. (1991) The role of the chloroplast in inorganic carbon acquisition by Chlamydomonas reinhardtii. Can. J. Bot. 69, 1017–1024

    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. 77, 177–183

    Google Scholar 

  • Moroney, J.V., Husic, H.D., Tolbert, N.E., Kitayama, M., Manuel, L.J., Togasaki, R.K. (1989) Isolation and characterization of a mutant of Chlamydomonas reinhardtii deficient in the CO2 concentrating mechanism. Plant Physiol. 89, 897–903

    Google Scholar 

  • Palmqvist, K., Sjöberg, S., Samuelsson, G. (1988) Induction of inorganic carbon accumulation in the unicellular green algae Scenedesmus obliquus and Chlamydomonas reinhardtii. Plant Physiol. 87, 437–441

    Google Scholar 

  • 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, 267–276

    Google Scholar 

  • Palmqvist, K., Ramazanov, Z.M., Gardeström, P., Samuelsson G. (1990b) Adaptation mechanism in microalgae to conditions of carbon dioxide-limited photosynthesis. Possible role of carbonic anhydrase. Fiziol. Rast. 37, 912–920

    Google Scholar 

  • Palmqvist, K., Ramazanov, Z., Samuelsson, G. (1991) Carbonic anhydrase in inorganic carbon assimilation in Dunaliella salina. Fiziol. Rast. 38, 465–473

    Google Scholar 

  • Ramazanov, Z., Semenenko, V.E. (1984) Oxygen-dependent induction of synthesis of the CO2-dependent soluble form of carbonic anhydrase in Chlorella cells. Sov. Plant Physiol. 31, 344–349

    Google Scholar 

  • Ramazanov, Z., 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, 340–344

    Google Scholar 

  • Ramazanov, Z., Cardenas, J.T. (1992) Inorganic carbon across cell compartments of the halotolerant alga Dunaliella salina. Physiol. Plant. 85, 121–128

    Google Scholar 

  • Ramazanov, Z., Mason, C.B., Geraghty, A.M., Spaldig, M.H., Moroney, J.V. (1993) The low CO2-inducible 36-kilodalton protein is localized to the chloroplast envelope of Chlamydomonas reinhardtii. Plant Physiol. 101, 1195–1199

    Google Scholar 

  • 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, Rockville

    Google Scholar 

  • Rawat, M., Moroney, J.V. (1991) Partial characterization of a new isoenzyme of carbonic anhydrase isolated from Chlamydomonas reinhardtii. J. Biol. Chem. 266, 9719–9723

    Google Scholar 

  • Samuelsson, G., Palmqvist, K., Ramazanov, Z., Sundblad, L.-G. (1990) Photosynthetic acclimation to low carbon concentrations in Chlamydomonas reinhardtii. In: Current research in photosynthesis, vol. IV. pp. 18441–18448, Baltscheffsky M., ed. Kluver Academic Publishers, Dordrecht

    Google Scholar 

  • Serrano, R. (1989) Structure and function of plasma membrane ATPase Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 61–94

    Google Scholar 

  • Solter, K.M., Gibor, A. (1977) The release of carbohydrates during mating in Chlamydomonas reinhardtii. Plant Sci Lett 8, 227–231

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Surzycki, S.J. (1971) Synchronously grown cultures of Chlamydomonas reinhardtii. Methods Enzymol. 23, 67–73

    Google Scholar 

  • Sültemeyer, D.F., Klöck, G., Kreuberg, K., Fock, H. (1988) Photosynthesis and apparent affinity for dissolved inorganic carbon by cells and protoplasts of Chlamydomonas reinhardtii grown at high and low CO2 concentrations. Planta 176, 256–260

    Google Scholar 

  • Sültemeyer, D.F., Fock, H.P., Canvin, D.T. (1990) Mass spectrometric measurement of intracellular carbonic anhydrase activity in high and low DIC cells of Chlamydomonas. Studies using 18O exchange with 13C/18O labeled bicarbonate. Plant Physiol. 94, 1250–1257

    Google Scholar 

  • Thielmann, J., Tolbert, N.E., Goyal, A., Senger, H. (1990) Two systems for concentrating CO2 and bicarbonate during photosynthesis by Scenedesmus. Plant Physiol. 92, 622–629

    Google Scholar 

  • Togasaki, R.K., Brunke, K., Kitayama, M., Griffin, M. (1987) Isolation of intact chloroplasts from Chlamydomonas reinhardtii with Beckman centrifugal elutriation. Prog. Photosynth. Res., 3, 499–502

    Google Scholar 

  • Williams, T.G., Turpin, D.H. (1987) The role of external carbonic anhydrase in inorganic carbon acquisition by Chlamydomonas reinhardtii at alkaline pH. Plant Physiol. 83, 92–96

    Google Scholar 

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We are grateful to Prof. J Cardenas (Dept de Bioquimica y Biologia Moleculary Fisiologia, University of Cordoba, Spain) and Prof. J.V. Moroney (Dept of Botany, Louisiana State University, USA) for critically reading the manuscript. We are also grateful to Gunilla Malmberg for expert assistance in the measurements of ATP/ADP ratios and Dr. C. Santos (The University of Cordoba, Spain) for skiful secretarial assistance. This work was supported by the Swedish Natural Research Council, Seth M. Kempes Memorial foundation and the Swedish Institute.

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Karlsson, J., Ramazanov, Z., Hiltonen, T. et al. Effect of vanadate on photosynthesis and the ATP/ADP ratio in low-CO2-adapted Chlamydomonas reinhardtii cells. Planta 192, 46–51 (1993). https://doi.org/10.1007/BF00198691

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