Abstract
It has been proposed that many marine macroalgae are able to utilize HCO −3 for photosynthesis and growth, and that energy-dependent ion pumping is involved in this process. We have therefore studied the light-dependent alkalization of the surrounding medium by two species of marine macroscopic brown algae, Fucus serratus L. and Laminaria saccharina (L.) Lamour. with the aim of investigating the role of extracellular carbonic anhydrase (EC 4.2.1.1.) in the assimilation of inorganic carbon from the seawater medium. In particular, the influence of membrane-impermeable or slowly permeable carbonic-anhydrase inhibitors on the rate of alkalization of the seawater has been investigated. Inhibition of the alkalization rate occurred in both species at an alkaline pH (pH 8.0) but no inhibition was observed at an acidic pH (pH 6.0). The alkalization was found to be light-dependent and inhibited by 3-(3′,4′-dichlorophenyl)-1, 1-dimethylurea and, thus, correlated with photosynthesis. Alkalization by macroalgae has previously been shown to be proportional to inorganiccarbon uptake. We suggest that alkalization of the medium at alkaline pH in both of the species examined is mainly the consequence of an extracellular reaction. The reaction is catalyzed by extracellular carbonic anhydrase which converts HCO −3 to OH− and CO2; CO2 is then taken up through the plasmalemma. However, we do not exclude the involvement of other mechanisms of inorganic-carbon uptake.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- AZ:
-
acetazolamide
- CA:
-
carbonic anhydrase
- CAext:
-
extracellular carbonic anhydrase
- Ci :
-
inorganic carbon
- DBS:
-
dextran-bound sulfonamide
- DCMU:
-
3-(3′,4′-dichloro-phenyl)-1,1-dimethylurea
- PPFD:
-
photosynthetic photon flux density
References
Axelsson, L. (1988) Changes in pH as a measure of photosynthesis by marine macroalgae. Mar. Biol. 97, 287–294
Axelsson, L., Uusitalo, J. (1988) Carbon acquisition strategies for marine macroalgae I. Utilization of proton exchanges visualized during photosynthesis in a closed system. Mar. Biol. 97, 295–300
Axelsson, L., Carlberg, S., Ryberg, H. (1989) Adaptions by macroalgae to low carbon availability. II. Ultrastructural specializations, related to the function of a photosynthetic buffer system in the Fucaceae. Plant Cell. Environ. 12, 771–778
Beardall, J. (1981) CO2 accumulation by Chlorella saccharophila (Chlorophyceae) at low external pH: evidence for active trans-port of inorganic carbon at the chloroplast envelope. J. Phycol. 17, 371–373
Beer, S., Israel, A. (1990) Photosynthesis of Ulva fasciata. IV, carbonic anhydrase and inorganic carbon conversions in the unstirred layer. Plant Cell Environ. 13, 555–560
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., Haglund, K., Ramazanov, Z., García-Reina, G., Pedersén, M. (1992) Inorganic carbon assimilation in the green seaweed Ulva rigida (Chlorophyta). Planta 187, 142–151
Bréchignac, F., André, M., Gerbaud, A. (1986) Preferential uptake of exogenous HCO −3 in the marine macroalga Chondrus crispus. Plant Physiol. 80, 1059–1062
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
Gehl, K.A., Colman, B., Sposato, L.M. (1990) Mechanism of inorganic carbon uptake in Chlorella saccharophila: The lack of involvement of carbonic anhydrase. J. Exp. Bot. 41 (232), 1385–1391
Giordano, M., Maberly, S.C. (1989) Distribution of carbonic anhydrase in British marine macroalgae. Oecologia 81, 534–539
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., Björk, M., Ramazanov, Z., García-Reina, G., Pedersén, M. (1992) Role of carbonic anhydrase in photosynthesis and inorganic carbon assimilation in the red alga Gracilaria tenuistipitata. Planta 187, 275–281
Jolliffe, E.A., Tregunna, E.B. (1970) Studies on HCO −3 ion uptake during photosynthesis in benthic marine algae. Phycologia 9, 293–303
Johnston, A.M. (1991) The acquisition of inorganic carbon by marine macroalgae. Can. J. Bot. 69, 1123–1132
Johnston, A.M., Raven, J.A. (1986) The utilization of bicarbonateions by the macroalga Ascophyllum nodosum (L.) Le Jolis. Plant Cell Environ. 9, 175–184
Kerby, N.W., Raven, J.A. (1985) Transport and fixation of inorganic carbon by marine algae. Adv. Bot. Res. 11, 71–123
King, R.J., Schramm, W. (1976) Photosynthetic rates of benthic marine algae in relation to light intensity and seasonal variations. Mar. Biol. 37, 215–222
Lignell, Å., Pedersén, M. (1989) Effect of pH and inorganic carbon concentrations on growth of Gracilaria secundata. Br. Phycol. J. 24, 83–89
Lindahl, P.E.B. (1963) The inhibition of photosynthesis of aquatic plants by tetramethylthiuram disulphide. Symb. Bot. Ups. 17, 1–47
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., 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
Raven, J.A., Johnston, A.M., MacFarlane, J.J. (1990) Carbon metabolism. In: Biology of the red algae, pp. 171–219, Cole K.M., Sheath, R.G., eds., Cambridge University Press, Cambridge New York Melbourne
Rotatore, C., Colman, B. (1991) The localization of active inorganic carbon transport at the plasma membrane in Chlorella ellipsoidea. Can. J. Bot. 69, 1025–1031
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. (1989) Mechanism of photosynthetic carbon dioxide uptake by the red macroalga, Chondrus crispus. Plant Physiol. 89, 93–99
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
Surif, M.B., Raven, J. (1989) Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and the Laminariales (Phaeophyta): ecological and taxonomic implications. Oecologia 78, 97–105
Thomas, E.A., Tregunna, E.B. (1968) Bicarbonate ion assimilation in photosynthesis by Sargassum muticum. Can. J. Bot. 46, 411–415
Wilbur, K.M., Anderson, N.G. (1948) Electrometric and colorimetric determination of carbonic anhydrase. J. Biol. Chem. 176, 147–154
Author information
Authors and Affiliations
Additional information
This study was carried out with financial support by SAREC (Swedish Agency for Research Cooperation with Developing Countries), Carl Trygger's Fund for Scientific Research (Sweden), SJFR (Swedish Council for Forestry and Agricultural Research) and CICYT (Spain). Z. Ramazanov is an invited professor of Ministerio de Educación y Ciencia, Spain.
Rights and permissions
About this article
Cite this article
Haglund, K., Ramazanov, Z., Mtolera, M. et al. Role of external carbonic anhydrase in light-dependent alkalization by Fucus serratus L. and Laminaria saccharina (L.) Lamour. (Phaeophyta). Planta 188, 1–6 (1992). https://doi.org/10.1007/BF00198932
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00198932