Skip to main content
SpringerLink
Log in

Effect of external CO2 concentrations on protein synthesis in the green algae Scenedesmus obliquus (Turp.) Kütz and Chlorella vulgaris (Kosikov)

  • Published:
Planta Aims and scope Submit manuscript

Abstract

Unicellular algae grown under low-CO2 conditions (0.03% CO2) have developed a means of concentrating CO2 at the site of ribulose-1,5-bisphosphate carboxylase/oxygenase. Cells with the CO2-concentrating mechanism (CCM) acquire the ability to accumulate inorganic carbon to a level higher than that obtained by simple diffusion. To identify proteins which are involved in the organization of the CCM, cells of Scenedesumus obliquus and Chlorella vulgaris grown in high CO2 (5% CO2 in air) were transferred to low-CO2 (0.03%) conditions in the presence of 35SO sup2−inf4 and, thereafter, polypeptides labeled with 35S were detected. Under low-CO2 conditions the inducton of 36-, 39-, 94- and 110- to 116kDa polypeptides were particularly observed in S. obliquus and 16-, 19-, 27-, 36-, 38- and 45-kDa polypeptides were induced in C. vulgaris. Western blots with antibodies raised against 37-kDa subunits of the periplasmic carbonic anhydrase (CA) of Chlamydomonas reinhardtii showed immunoreactive bands with the 39-kDa polypeptide in the whole-cell homogenates from S. obliquus and with 36 and 38-kDa polypeptides in both high- and low-CO2grown cells of C. vulgaris. Anti-pea-chloroplast CA antibodies cross-reacted with a single polypeptide of 30 kDa in the whole-cell homogenates but not with thylakoid membranes. The CA activity was associated with soluble and membrane-bound fractions, except thylakoid membranes.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

CA:

carbonic anhydrase

CCM:

CO2-concentrating mechanism

DIC:

dissolved inorganic carbon (CO2 + HCO sup−inf3 + CO sup2−inf3 )

Rubisco:

ribulose-1,5-bisphosphatecarboxylase/oxygenase

References

  • Aizawa, K., Miyachi, S. (1986) Carbonic anhydrase and CO2 concentrating mechanisms in microalgae and cyanobacteria. FEMS Microbiol. Rev. 39, 215–233

    Google Scholar 

  • Badger, M.R., Price G.D. (1992) The CO2 concentrating mechanism in cyanobacteria and microalgae. Physiol. Plant 84, 606–615

    Google Scholar 

  • Badger, M.R., Price, G.D. (1994) The role of carbonic anhydrase in photosynthesis. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 45, 369–392

    Google Scholar 

  • 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 saccharophilla (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 

  • Bradford, M.M. (1976) Arapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254

    Google Scholar 

  • Coleman, J.R. (1992) The molecular and biochemical analysis of CO2-concentrating mechanism in cyanobacteria and microalgae. Plant Cell Environ. 14, 861–867

    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., Rotatore, 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. (1977) Correlation between accessibility of carbonic anhydrase for external substrate and regulation of photosynthetic use of CO2 and HCO sup−3 by Scenedesmus obliquus. Z. Pflanzenphysiol. 79, 428–437

    Google Scholar 

  • Fujiwara, S., Fukuzawa, H., Tachiki, A., Miyachi, S. (1990) Structure and differential expression of two genes encoding carbonic anhydrase in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 87, 9779–9783

    Google Scholar 

  • Fukuzawa, H., Fujiwara, S., Yamamoto, Y., Dionisio-Sese, M.L., Miyachi, S. (1990) cDNA cloning, sequence and expression of carbonic anhydrase in Chlamydomonas reinhardtii: Regulation by environmental CO2 concentration. Proc. Natl. Acad. Sci. USA 87, 4383–4387

    Google Scholar 

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

    Google Scholar 

  • Goyal, A., Shiraiwa, Y., Husic, H.D., Tolbert, N.E. (1992) External and internal carbonic anhydrase in Dunaliella species. Mar. Biol. 113, 349–355

    Google Scholar 

  • Husic, H.D., Marcus, C.A. (1994) Identification of intracellular carbonic anhydrase in Chlamydomonas reinhardtii with a carbonic anhydrase-directed photoaffinity label. Plant Physiol. 105, 133–139

    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 

  • Kaplan, A., Shwartz, R., Lieman-Hurwitz, J., Reinhold, L. (1991) Physiological and molecular aspects of the inorganic carbonconcentrating mechanism in cyanobacteria. Plant Physiol. 97, 851–855

    Google Scholar 

  • Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685

    PubMed  Google Scholar 

  • Manuel, L.J., Moroney, J.V. (1988) Inorganic carbon accumulation in Chlamydomonas reinhardtii: New proteins are made during adaption to low CO2. Plant Physiol. 88, 491–496

    Google Scholar 

  • Martínez, F., Villarejo, A., Ramazanov, Z., Orus, M.I. (1992) Carbonic anhydrase independent stimulation of inorganic carbon fixation mediated by glucose. In: Research in photosynthesis, vol. 3, pp. 803–806, Murata, N., ed. Kluwer Academic Publishers, The Netherlands

    Google Scholar 

  • Metz, J.G., Seibert, M. (1984) Presence in photosystem II core complexes of a 34-kilodalton polypeptide required for water photolysis. Plant Physiol. 76, 829–832

    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 

  • Moubarak-Milad, M., Stemler, A. (1994) Oxidation-reduction potential dependence of photosystem II carbonic anhydrase in maize thylakoids. Biochemistry 33, 4432–4438

    Google Scholar 

  • Palmqvist, K., Ramazanov, Z., Gardestöm, P., Samuelsson, G. (1990) The role of extracellular carbonic anhydrase for accumulation of inorganic carbon in the green alga Chlamydomonas reinhardtii. Physiol. Plant. 80, 267–276

    Google Scholar 

  • Pesheva, I., Ramazanov, Z., Semenenko, V. (1988) A study on light-induced activity of carbonic anhydrase in Scenedesmus cells. In: Proceedings of the international symposium on plant mineral nutrition and photosynthesis, vol.15, pp. 341–344, Ivanov, G., ed. The Bulgarian Academy of Sciences, Sofia

    Google Scholar 

  • Pronina, N., Semenenko, V.E. (1990) Localization of bound carbonic anhydrase in membranes of Chlorella cells. Fizil. Rasten. (Moscow) 31, 241–249

    Google Scholar 

  • Pronina, N., Ramazanov, Z., Semenenko, V.E. (1981) Carbonic anhydrase activity of Chlorella cells as a function of CO2 concentration. Fiziol. Rasten. (Moscow) 31, 344–352

    Google Scholar 

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

    Google Scholar 

  • Ramazanov, Z., Cárdenas, J. (1994) Photorespiratory ammonium assimilation in chloroplast of Chlamydomonas reinhardtii. Physiol. Plant. 90, 495–502

    Google Scholar 

  • Ramazanov, Z., Mason, C., Geraghty, A., Spalding, M., Moroney, J. (1993) The low CO2-inducible 36-kilodalton protein is localized to the chloroplast envelope of Chlamydomonas reinhardtii Plant Physiol. 101, 1195–1999

    Google Scholar 

  • Ramazanov, Z., Sosa, P., Henk, C.M., Jiménez del Río, M., Gómez Pinchetti, J.L., García Reina, G. (1994) Low CO2 inducible protein synthesis in the green alga Dunaliella tertiolecta. Planta 195, 519–524

    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 

  • Semenenko, V., Avramova, S., Georgiev, D., Pronina, N. (1977) Comparative study of activity and localization of carbonic anhydrase in cells of Chlorella and Scenedesmus. Fiziol. Rasten. (Moscow) 24, 1055–1059

    Google Scholar 

  • Shiraiwa, Y., Miyachi, S. (1985) Effect of temperature and CO2 concentration on induction of carbonic anhydrase and changes in efficiency of photosynthesis in Chlorella vulgaris 11 h. Plant Cell Physiol. 26, 543–549

    Google Scholar 

  • Shiraiwa, Y., Umino, Y. (1991) Effect of glucose on the induction of the carbonic anhydrase and the change in K1/2 (CO2) of photosynthesis in Chlorella vulgaris 11 h. Plant Cell Physiol. 32, 311–314

    Google Scholar 

  • Shiraiwa, Y., Yokoyama, S., Satoh, A. (1991) pH-dependent regulation of carbonic anhydrase induction and change in photosynthesis during adaptation of Chlorella cells to low CO2. Jpn. J. Phycol. 39, 355–362

    Google Scholar 

  • Spalding, M.H., Jeffrey M. (1989) Membrane-associated polypeptides induced in Chlamydomonas reinhardtii by limiting CO2 concentration. Plant Physiol. 89, 133–137

    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., Winder, T.L., Anderson, J.C., Geraghty, A.M., Marek, L.F. (1991) Changes in protein and gene expression during induction of the CO2-concentrating mechanism in wild-type and mutant Chlamydomonas. Can. J. Bot. 69, 1008–1016

    Google Scholar 

  • Stemler, A. (1993) An assay for carbonic anhydrase activity and reactions that produce radiolabeled gases of small uncharged molecules. Anal. Biochem. 210, 328–331

    Google Scholar 

  • Sueoka, M. (1960) Mitotic replication of deoxyribonucleic acids in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 46, 83–91

    Google Scholar 

  • Sültemeyer, D., Schmidt, C., Fock, H.P. (1993) Carbonic anhydrases in higher plants and aquatic microorganisms. Physiol. Plant. 88, 179–190

    Google Scholar 

  • Suzuki, E., Shiraiwa, Y., Miyachi, S. (1994) The cellular and molecular aspects of carbonic anhydrase in photosynthetic microorganisms. In: Progress in physiological research, eds. Round, F.E., Chapman, D.J., eds. Biopress Ltd, Bristol, UK (in press).

    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

    CAS  PubMed  Google Scholar 

  • Tsuzuki, M., Miyachi, S. (1991) CO2 syndrome in Chlorella. Can. J. Bot. 69, 1003–1007

    Google Scholar 

  • Williams, T.G., Colman, B. (1993) Identification of distinct internal and external isoenzymes of carbonic anhydrase in Chlorella saccharophila Plant Physiol. 103, 943–948

    Google Scholar 

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

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Applied Algology, Technological Institute of the Canary Islands, Muelle de Taliarate s/n 35214, Telde, Las Palmas, Spain

    Ziyadin Ramazanov, Miguel Jiménez del Río & Jorge Rubio

  2. Department of Biology, Faculty of Science, Niigata University, Niigata 950-21, Japan

    Yoshihiro Shiraiwa

Authors
  1. Ziyadin Ramazanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yoshihiro Shiraiwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Miguel Jiménez del Río
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jorge Rubio
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

The authors are grateful to Prof. S. Bartlett (Louisiana State University, USA) for the gift of antibodies against spinach Rubisco and to Prof. J. Coleman (University of Toronto, Canada) for providing pea chloroplast CA antibodies. We thank Dr. J. Moroney (Louisiana State University, USA) for providing antibodies against the 37-kDa subunits of periplasmic CA of C. reinhardtii. We thank Prof. D. Müller (University of Konstanz, Germany) and Dr. Flor Martínez (Universidad Autónoma de Madrid, Spain) for their critical contribution to the manuscript. This work was supported by Instituto Tecnológico de Canarias (Spain).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ramazanov, Z., Shiraiwa, Y., del Río, M.J. et al. Effect of external CO2 concentrations on protein synthesis in the green algae Scenedesmus obliquus (Turp.) Kütz and Chlorella vulgaris (Kosikov). Planta 197, 272–277 (1995). https://doi.org/10.1007/BF00202647

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00202647

Key words

Search

Navigation