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.
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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
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
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
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
Bidwell, R.G.S., McLachlan, J. (1985) Carbon nutrition of seaweeds: photosynthesis, photorespiration and respiration. J. Exp. Mar. Biol. Ecol. 86, 15–46
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
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
Bowes, G.W. (1969) Carbonic anhydrase in marine algae. Plant Physiol. 44, 726–732
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
Burns, B.D., Beardall, J. (1988) Utilization of inorganic carbon by marine microalgae. J. Exp. Mar. Biol. Ecol. 107, 75–86
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
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
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
Enns, T. (1967) Facilitation by carbonic anhydrase of carbon dioxide transport. Science 155, 44–47
Giordano, M., Maberly, S.C. (1989) Distribution of carbonic anhydrase in British marine macroalgae. Oecologia 81, 534–539
Graham, D., Smillie, R.M. (1976) Carbonate dehydratase in marine organisms of the Great Barrier Reef. Aust. J. Plant Physiol. 3, 113–119
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
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
Johnson, K.S. (1982) Carbon dioxide hydration and dehydration kinetics in seawater. Limnol. Oceanogr. 27, 849–855
Jolliffe, E.A., Tregunna, E.B. (1970) Studies on HCO −3 ion uptake during photosynthesis in benthic marine algae. Phycologia 9, 293–303
Kerby, N.W., Raven, J.A. (1985) Transport and fixation of inorganic carbon by marine algae. Adv. Bot. Res. 11, 71–123
Lindahl, P.E.B. (1963) The inhibition of the photosynthesis of aquatic plants by tetramethylthiuram disulphide. Symbolae Bot. Upsalienses 17, 1–47
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
Lignell, Å., Pedersén, M. (1989) Effects of pH and inorganic carbon concentrations on growth of Gracilaria secundata. Br. Phycol. J. 24, 83–89
Lucas, W.J. (1983) Photosynthetic assimilation of exogenous HCO −3 by aquatic plants. Annu. Rev. Plant Physiol. 34, 71–104
Maberly, S.C. (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J. Phycol. 26, 439–449
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
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
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
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
Peterson, G.L. (1983) Determination of total protein. Methods Enzymol. 91, 95–119
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
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
Reiskind, J.B., Seamon, P.T., Bowes, G. (1988) Alternative methods of photosynthetic carbon assimilation in marine macroalgae. Plant Physiol. 87, 686–692
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
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
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
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
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
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
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
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
Tinker, J.P., Coulson, R., Weiner, I.M. (1981) Dextran-bound inhibitors of carbonic anhydrase. J. Pharmacol. Exp. Ther. 218, 600–607
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
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
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
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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.
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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
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DOI: https://doi.org/10.1007/BF00201951