Skip to main content
SpringerLink
Log in

Role of carbonic anhydrase in photosynthesis and inorganic-carbon assimilation in the red alga Gracilaria tenuistipitata

  • Published:
Planta Aims and scope Submit manuscript

Abstract

The mechanism of inorganic-carbon (Ci) accumulation in the red seaweed Gracilaria tenuistipitata Zhang et Xia has been investigated. Extracellular and intracellular carbonic-anhydrase (CA) activities have been detected. Photosynthetic O2 evolution in thalli and protoplasts of G. tenuistipitata were higher at pH 6.5 than at pH 8.6, where HCO −3 is the predominant form of Ci. Dextran-bound sulfonamide (DBS), a specific inhibitor of extracellular CA, reduced photosynthetic O2 evolution at pH 8.6 and did not have any effect at pH 6.5. After inhibition with DBS, O2 evolution was similar to the rate that could be supported by CO2 from spontaneous dehydration of HCO −3 . The rate of photosynthetic alkalization of the surrounding medium by the algal thallus was dependent on the concentration of Ci and inhibited by DBS. We suggest that the general form of Ci that enters through the plasma membrane of G. tenuistipitata is CO2. Bicarbonate is utilized mainly by an indirect mechanism after dehydration to CO2, and this mechanism involves extracellular CA.

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

Ci :

inorganic carbon (CO2 + HCO −3 )

CA:

carbonic anhydrase

DIC:

dissolved inorganic carbon (total)

DBS:

dextran-bound sulfonamide

EZ:

ethoxyzolamide

NSW:

natural seawater

PPFD:

photosynthetic photon flux density

REA:

relative enzyme activity

Rubisco:

ribulose-1,5-bisphosphate carboxylase/oxygenase

References

  • Axelsson, L. (1988) Changes in pH as a measure of photosynthesis by marine macroalgae. Mar. Biol. 97, 287–294

    Google Scholar 

  • Beardall, J. (1981) CO2 accumulation by Chlorella saccharophila (Chlorophyceae) at low external pH: evidence for active transport of inorganic carbon at the chloroplast envelope. J. Phycol. 17, 371–373

    Google Scholar 

  • Beer, S., Israel, A. (1990) Photosynthesis of Ulva fasciata IV. pH, carbonic anhydrase, and inorganic carbon conversions in the unstirred layer. Plant Cell Environ. 13, 555–60

    Google Scholar 

  • Beer, S., Israel, A., Drechsler, Z., Cohen, Y. (1990) Photosynthesis in Ulva fasciata V. Evidence for an inorganic carbon concentrating system, and ribulose-1,5-bisphosphate carboxylase/ oxygenase CO2 kinetics. Plant Physiol. 94, 1542–1546

    Google Scholar 

  • Bidwell, R.G.S., McLachlan, J. (1985) Carbon nutrition of seaweeds: photosynthesis, photorespiration and respiration. J. Exp. Mar. Biol. Ecol. 86, 15–46

    Google Scholar 

  • Björk, M., Ekman, P., Wallin, A., Pedersén, M. (1990) Effects of growth rate and other factors on protoplast yield from four species of the red seaweed Gracilaria (Rhodophyta). Bot. Mar. 33, 433–439

    Google Scholar 

  • Björk, M., Haglund, K., Ramazanov, Z., García-Reina, G., Pedersén, M. (1992) Inorganic carbon assimilation in the green seaweed Ulva rigida (Chlorophyta). Planta 187, 152–156

    Google Scholar 

  • Bowes, G.W. (1969) Carbonic anhydrase in marine algae. Plant Physiol. 44, 726–732

    Google Scholar 

  • Bréchignac, F., André, M., Gerbaud, A. (1986) Preferential photosynthetic uptake of exogenous HCO −3 in the marine macroalga Chondrus crispus. Plant Physiol. 80, 1059–1062

    Google Scholar 

  • Burns, B.D., Beardall, J. (1988) Utilization of inorganic carbon by marine microalgae. J. Exp. Mar. Biol. Ecol. 107, 75–86

    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 

  • Cook, C.M., Lanaras, T., Colman, B. (1986) Evidence for bicarbonate transport in species of red and brown macrophytic marine algae. J. Exp. Bot. 37, 977–984

    Google Scholar 

  • Cook, C.M., Lanaras, T., Roubelakis-Angelakis, K.A. (1988) Bicarbonate transport and alkalization of the medium by four species of Rhodophyta. J. Exp. Bot. 39, 1185–1198

    Google Scholar 

  • Enns, T. (1967) Facilitation by carbonic anhydrase of carbon dioxide transport. Science 155, 44–47

    Google Scholar 

  • Giordano, M., Maberly, S.C. (1989) Distribution of carbonic anhydrase in British marine macroalgae. Oecologia 81, 534–539

    Google Scholar 

  • Graham, D., Smillie, R.M. (1976) Carbonate dehydratase in marine organisms of the Great Barrier Reef. Aust. J. Plant Physiol. 3, 113–119

    Google Scholar 

  • Gutknecht, J., Bisson, M.A., Tosteson, F.C. (1977) Diffusion of carbon dioxide through lipid bilayer membranes. Effects of carbonic anhydrase, bicarbonate and unstirred layers. J. Gen. Physiol. 69, 779–794

    Google Scholar 

  • Haglund, K., Axelsson, L., Pedersén, M. (1987) Photosynthesis and respiration in the alga Ahnfeltia plicata in a flow-through system. Mar. Biol. 96, 409–412

    Google Scholar 

  • Johnson, K.S. (1982) Carbon dioxide hydration and dehydration kinetics in seawater. Limnol. Oceanogr. 27, 849–855

    Google Scholar 

  • Jolliffe, E.A., Tregunna, E.B. (1970) Studies on HCO −3 ion uptake during photosynthesis in benthic marine algae. Phycologia 9, 293–303

    Google Scholar 

  • Kerby, N.W., Raven, J.A. (1985) Transport and fixation of inorganic carbon by marine algae. Adv. Bot. Res. 11, 71–123

    Google Scholar 

  • Lindahl, P.E.B. (1963) The inhibition of the photosynthesis of aquatic plants by tetramethylthiuram disulphide. Symbolae Bot. Upsalienses 17, 1–47

    Google Scholar 

  • Lignell, Å., Ekman, P., Pedersén, M. (1987) Cultivation technique for marine seaweeds allowing controlled and optimized conditions in the laboratory and on a pilotscale. Bot. Mar. 30, 417–424

    Google Scholar 

  • Lignell, Å., Pedersén, M. (1989) Effects of pH and inorganic carbon concentrations on growth of Gracilaria secundata. Br. Phycol. J. 24, 83–89

    Google Scholar 

  • Lucas, W.J. (1983) Photosynthetic assimilation of exogenous HCO −3 by aquatic plants. Annu. Rev. Plant Physiol. 34, 71–104

    Google Scholar 

  • Maberly, S.C. (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J. Phycol. 26, 439–449

    Google Scholar 

  • Moroney, J.V., Husic, D.H., 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., Kitayama, M., Tokasaki, R.K., Tolbert, N.E. (1987) Evidence for inorganic carbon transport by intact chloroplasts of Chlamydomonas reinhardtii. Plant Physiol. 83, 460–463

    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., Gardeström, P., Samuelsson, G. (1990b) Adaption mechanisms in microalgae to conditions of carbon dioxide-limited photosynthesis. Possible role of carbonic anhydrase. Fiziol. Rast. (Moscow) 37, 912–920

    Google Scholar 

  • Peterson, G.L. (1983) Determination of total protein. Methods Enzymol. 91, 95–119

    Google Scholar 

  • Provasoli, L. (1968) Media and prospects for the cultivation of marine algae. In: Cultures and Collections of Algae (Proc. US-Japan Conf., Hakone), pp. 63–75, Watanabe, A., Hattori, A., eds. Jpn. Soc. Plant Physiol.

  • Ramazanov, Z.M., 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 

  • 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. Rockwell, Maryland

    Google Scholar 

  • Reiskind, J.B., Seamon, P.T., Bowes, G. (1988) Alternative methods of photosynthetic carbon assimilation in marine macroalgae. Plant Physiol. 87, 686–692

    Google Scholar 

  • Sand-Jensen, K., Gordon, D.M. (1984) Differential ability of marine and freshwater macrophytes to utilize HCO −3 and CO2. Mar. Biol. 80, 247–253

    Google Scholar 

  • Skirrow, G. (1975) The dissolved gases — carbon dioxide. In: Chemical oceanography, vol. 2, pp. 1–192, Riley, J.P., Skirrow, G., eds. Academic Press, London New York San Francisco

    Google Scholar 

  • Smith, R.G., Bidwell, R.G.S. (1987) Carbonic anhydrase-dependent inorganic carbon uptake by the red macroalga, Chondrus crispus. Plant Physiol. 83, 735–738

    Google Scholar 

  • Smith, R.G., Bidwell, R.G.S. (1989a) Mechanism of photosynthetic carbon dioxide uptake by the red macroalga, Chondrus crispus. Plant Physiol. 89, 93–99

    Google Scholar 

  • Smith, R.G., Bidwell, R.G.S. (1989b) Inorganic carbon uptake by photosynthetically active protoplasts of the red macroalga Chondrus crispus. Mar. Biol. 102, 1–44

    Google Scholar 

  • Sültemeyer, D.F., Miller, A.G., Espie, G.S., Fock, H.P., Canvin, D.T. (1989) Active CO2 transport by the green alga Chlamydomonas reinhardtii. Plant Physiol. 89, 1213–1219

    Google Scholar 

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

    Google Scholar 

  • Surif, M.B., Raven, J.A. (1989) Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and Laminariales (Phaeophyta): ecological and taxonomic implications. Oecologia 78, 97–105

    Google Scholar 

  • Tinker, J.P., Coulson, R., Weiner, I.M. (1981) Dextran-bound inhibitors of carbonic anhydrase. J. Pharmacol. Exp. Ther. 218, 600–607

    Google Scholar 

  • Tseng, C.K., Sweeney, B.M. (1946) Physiological studies of Gelidium cartilagineum. I. Photosynthesis, with special reference to the carbon dioxide factor. Am. J. Bot. 33, 706–715

    Google Scholar 

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

    Google Scholar 

  • Yagawa, Y., Muto, S., Miyachi, S. (1987) Carbonic anhydrase of a unicellular red alga Porphyridium cruentum R-1. II. Distribution and role in photosynthesis. Plant Cell Physiol. 28, 1509–1516

    Google Scholar 

Download references

Author information

Author notes

  1. Ziyadin Ramazanov

    Present address: Department of Botany, Louisiana State University, 70803, Baton Rouge, Louisiana, USA

Authors and Affiliations

  1. Department of Physiological Botany, Uppsala University, P.O. Box 540, S-751 21, Uppsala, Sweden

    Kurt Haglund, Mats Björk & Marianne Pedersén

  2. Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya 35, 276, Moscow, Russian Federation

    Ziyadin Ramazanov

  3. Marine Plant Biotechnology Laboratory, University of Las Palmas, P.O. Box 550, E-35017, Las Palmas, Gran Canaria, Spain

    Guillermo García-Reina

Authors
  1. Kurt Haglund
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mats Björk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ziyadin Ramazanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guillermo García-Reina
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marianne Pedersén
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This research was supported by the Deutsche Forschungsgemeinschaft (Bonn) as a programme of the “Sonderforschungsbereich 251 der Universität Würzburg” and by the “Fonds der Chemischen Industrie” (Frankfurt). Joint work in Würzburg was possible thanks to travel grants from the Chancellor of the University of Würzburg, Professor R. Günther, from the Australian National University under the auspices of its Overseas Studies Programme, and from the New Zealand — Federal Republic of Germany Scientific and Technological Exchange Programme, which are gratefully acknowledged. We thank Dr. A. Meyer and Ms. E. Kilian for untiringly conducting part of the experimental work, Ms. G. Theumer and Ms. D. Faltenbacher-Werner for their valuable assistance, and Mr. H. Walz (Walz Company, Effeltrich, FRG) for his skilled help with the calibration of our gas-exchange system for measurements with helox. The Department of Conservation, New Zealand, is thanked for permission to collect lichens.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Haglund, K., Björk, M., Ramazanov, Z. et al. Role of carbonic anhydrase in photosynthesis and inorganic-carbon assimilation in the red alga Gracilaria tenuistipitata . Planta 187, 275–281 (1992). https://doi.org/10.1007/BF00201951

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00201951

Key words

Search

Navigation