Abstract
The metabolic pathway of primary carbon fixation was studied in a peculiar pennate marine diatom, Haslea ostrearia (Bory) Simonsen, which synthesizes and accumulates a blue pigment known as “marennine”. Cells were cultured in a semi-continuous mode under saturating [350 µmol(photon) m−2 s−1] or non-saturating [25 µmol(photon) m−2 s−1] irradiance producing “blue” (BC) and “green” (GC) cells, characterized by high and low marennine accumulation, respectively. Growth, pigment contents (chlorophyll a and marennine), 14C accumulation in the metabolites, and the carbonic anhydrase (CA) activity of the cells were determined during the exponential growth phase. Growth rate and marennine content were closely linked to irradiance during growth: higher irradiance increased both growth rate and marennine content. On the other hand, the Chl a concentration was lower under saturating irradiance. The distribution between the Calvin-Benson (C3) and β-carboxylation (C4) pathways was very different depending on the irradiance during growth. Metabolites of the C3 cycle contained about 70 % of the total fixed radioactivity after 60 s of incorporation into cells cultured under the non-saturating irradiance (GC), but only 47 % under saturating irradiance (BC). At the same time, carbon fixation by β-carboxylation was 24 % in GC versus about 41 % in BC, becoming equal to that in the C3 fixation pathway in the latter. Internal CA activity remained constant, but the periplasmic CA activity was higher under low than high irradiance.
Similar content being viewed by others
References
Badger, M.R., Price, G.D.: The CO2 concentrating mechanism in cyanobacteria and microalgae.-Physiol. Plant. 84: 606–615, 1992.
Badger, M.R., Price, G.D.: The role of carbonic anhydrase in photosynthesis.-Annu. Rev. Plant Physiol. Plant mol. Biol. 45: 369–392, 1994.
Beardall, J.: Photosynthesis and photorespiration in marine phytoplankton.-Aquat. Bot. 34: 105–130, 1989.
Beardall, J., Mukerji, D., Glover, H.E., Morris, I.: The path of carbon in photosynthesis by marine phytoplankton.-J. Phycol. 12: 409–417, 1976.
Birmingham, B.C., Coleman, J.R., Colman, C.: Measurement of photorespiration in algae.-Plant Physiol. 69: 259–262, 1982.
Coudret, A., Ferron, F., Jolivet, P., Tremblin, G., Bergeron, E., Sourie, M.C.: Fate of metabolites issued from 14C dark fixation into brown seaweeds; connection with their respective biology.-Photosynthetica 26: 235–245, 1992.
Cunningham, F.X., Jr., Vonshak, A., Gantt, E.: Photoacclimation in the red alga Porphyridium cruentum. Changes in photosynthetic enzymes, electron carriers, and light saturated rate of photosynthesis as a function of solar irradiance and spectral quality.-Plant Physiol. 100: 1142–1149, 1992.
Descolas-Gros, C., Oriol, L.: Variations in carboxylase activity in marine phytoplankton cultures. β-carboxylation in carbon flux studies.-Mar. Ecol. Prog. Ser. 85: 163–169, 1992.
Dionisio, M.L., Tsuzuki, M., Miyachi, S.: Light requirement for carbonic anhydrase induction in Chlamydomonas reinhardtii.-Plant Cell Physiol. 30: 207–213, 1989a.
Dionisio, M.L., Tsuzuki, M., Miyachi, S.: Blue light induction of carbonic anhydrase activity in Chlamydomonas reinhardtii.-Plant Cell Physiol. 30: 215–219, 1989b.
Geider, R.J., MacIntyre, H.L., Kana, T.M.: Dynamic model of phytoplankton growth and acclimation: Response to the balanced growth rate and the chlorophyll a:carbon ratio to light, nutrient limitation and temperature.-Mar. Ecol. Prog. Ser. 148: 187–200, 1997.
Glover, H.E.: Ribulosebisphosphate carboxylase/oxygenase in marine organisms.-Int. Rev. Cytol. 115: 67–137, 1989.
Graham, D., Reed, M.L., Patterson, B.D., Hockley, D.G.: Distribution and physiology of plant and algal carbonic anhydrases.-Ann. New York Acad. Sci. 429: 222–237, 1984.
Granum, E., Raven, J.A., Leegood, R.C.: How do marine diatoms fix 10 billion tonnes of inorganic carbon per year?-Can. J. Bot. 83: 898–908, 2005.
Haglund, K., Ramazanov, Z., Mtolera, M., Pedersén, M.: Role of external carbonic anhydrase in light-dependent alkalization by Fucus serratus L. and Laminaria saccharina (L.) Lamour (Phaeophyta).-Planta 188: 1–6, 1992.
Johnston, A.M., Raven, J.A., Beardall, J., Leegood, R.C.: Photosynthesis in a marine diatom.-Nature 412: 40–41, 2001.
Melis, A., Neidhardt, J., Benemann, J.R.: Dunaliella salina (Chlorophyta) with small chlorophyll antenna sizes exhibits higher photosynthetic productivities and photon use efficiencies than normally pigmented cells.-J. appl. Phycol. 10: 515–525, 1999.
Morant-Manceau, A., Nguyen, T.L.N., Pradier, E., Tremblin, G.: Carbonic anhydrase activity and photosynthesis in marine diatoms.-Eur. J. Phycol. 42: 1–8, 2007.
Morris, I.: Paths of carbon assimilation in marine phytoplankton.-In: Falkowski, P.G. (ed.): Primary Productivity in the Sea. Pp. 139–159. Plenum Press, New York 1980.
Mortain-Bertrand, A.: Influence des fluctuations lumineuses sur le métabolisme photosynthétique et la productivité de diatomées tempérées et antarctiques en culture.-Thèse Doct. Univ. Paris VI, Paris 1987.
Mortain-Bertrand, A., Descolas-Gros, C., Jupin, H.: Short-term 14C incorporation in Skeletonema costatum (Greville) Cleve (Bacillariophyceae) as a function of light regime.-Phycologia 26: 262–269, 1987.
Mouget, J.L., Tremblin, G., Morant-Manceau, A., Morançais, M., Robert, J.M.: Long-term photoacclimation of Haslea ostrearia (Bacillariophyta): Effect of irradiance on growth rates, pigment content and photosynthesis.-Eur. J. Phycol. 34: 109–115, 1999.
Nassiri, Y., Robert, J.M., Rincé, Y., Ginsburger-Vogel, T.: The cytoplasmic fine structure of the diatom Haslea ostrearia (Bacillariophyceae) in relation to marennine production.-Phycologia 37: 84–91, 1998.
Parker, M.S., Armbrust, E.V.: Synergistic effects of light, temperature, and nitrogen source on transcription of genes for carbon and nitrogen metabolism in the centric diatom Thalassiosira pseudonana (Bacillariophyceae).-J. Phycol. 41: 1142–1153, 2005.
Parker, M.S., Armbrust, E.V., Piovia-Scott, J., Keil, R.G.: Induction of photorespiration by light in the centric diatom Thalassiosira weissflogii (Bacillariophyceae): molecular characterization and physiological consequences.-J. Phycol. 40: 557–567, 2004.
Pouvreau, J.B., Morancais, M., Fleury, F., Rosa, P., Thion, L., Cahingt, B., Zal, F., Fleurence, J., Pondaven, P.: Preliminary characterization of the blue-green pigment “marennine” from the marine tychopelagic diatom Haslea ostrearia (Gaillon/Bory) Simonsen.-J. appl. Phycol. 18: 757–767, 2006.
Raven, J.A.: Photosynthetic and non-photosynthetic roles of carbonic anhydrase in algae and cyanobacteria.-Phycologia 34: 93–101, 1995.
Raven, J.A.: Inorganic carbon acquisition by marine autotrophs.-Adv. bot. Res. 27: 85–209, 1997.
Raven, J.A., Beardall, J.: Carbon acquisition mechanisms of algae: carbon dioxide diffusion and carbon dioxide concentrating mechanisms.-In: Larkum, A.W.D., Douglas, S.E., Raven, J.A. (ed.): Photosynthesis in Algae. Pp. 225–244. Kluwer Academic Publ., Dordrecht-Boston-London 2003.
Rech, M.: Effets de l’éclairement visible et ultraviolet sur la croissance et la photosynthèse de microalgues: incidences sur l’écophysiologie du phytoplankton des claires ostréicoles.-Thèse Doct. Univ. du Maine, Le Mans 2004.
Reinfelder, J.R., Kraepiel, A.M.L., Morel, F.M.: Unicellular C4 photosynthesis in a marine diatom.-Nature 407: 996–999, 2000.
Reinfelder, J.R., Milligan, A.J., Morel, F.M.M.: The role of the C4 pathway in carbon accumulation and fixation in a marine diatom.-Plant Physiol. 135: 2106–2111, 2004.
Riebesell, U.: Carbon fix for a diatom.-Nature 407: 959–960, 2000.
Riley, J.P., Chester, R.: The dissolved gases in sea water. Carbon dioxide.-In: Riley, J.P., Chester, R. (ed.): Introduction to Marine Chemistry. Pp. 121–151. Academic Press, London-New York 1971.
Rincé, Y.: Intervention des diatomées dans l’écologie des claires ostréicoles de la baie de Bourgneuf.-Thèse Doct. Univ. Nantes, Nantes 1978.
Robert, J.M.: Fertilité des eaux des claires ostréicoles et verdissement: Utilisation de l’azote par les diatomées dominantes.-Thèse Doct. Univ. Nantes, Nantes 1983.
Robert, J.M., Morançais, M., Pradier, E., Mouget, J.L., Tremblin, G.: Extraction, purification and spectrophotometric analysis of the blue pigment “marennine” produced by the diatom Haslea ostrearia.-J. appl. Phycol. 14: 299–305, 2002.
Schürmann, P.: Separation of phosphate esters and algal extracts by thin-layer electrophoresis and chromatography.-J. Chromatogr. 39: 507–509, 1969.
Shubert, H., Tremblin, G., Robert, J.M., Sagert, S., Rince, Y.: In vivo fluorescence measurement of photosynthesis of Haslea ostrearia in relation to marennine content.-Diatom Res. 10: 341–349, 1995.
Speziale, B.J., Schreiner, S.P., Giammatteo, P.A., Schindler, J.E.: Comparison of N,N-dimethylformamide, dimethyl sulfoxide, and acetone for extraction of phytoplankton chlorophyll.-Can. J. Fish. aquat. Sci. 41: 1519–1522, 1984.
Tremblin, G., Jolivet, P., Coudret, A.: Light quality effects on subsequent dark 14CO2-fixation in Fucus serratus.-Hydrobiologia 260/261: 471–475, 1993.
Tremblin, G., Robert, J.M.: Photosynthesis of Haslea ostrearia in relation with its blue pigmentation.-Compt. rend. Acad. Sci. Paris 319: 939–944, 1996.
Tremblin, G., Robert, J.-M.: Carbon fixation by the peculiar marine diatom Haslea ostrearia.-Photosynthetica 39: 215–220, 2001.
Zimba, P.V., Sullivan, M.J., Glover, H.E.: Carbon fixation in cultured marine benthic diatoms.-J. Phycol. 26: 306–311, 1990.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rech, M., Morant-Manceau, A. & Tremblin, G. Carbon fixation and carbonic anhydrase activity in Haslea ostrearia (Bacillariophyceae) in relation to growth irradiance. Photosynthetica 46, 56–62 (2008). https://doi.org/10.1007/s11099-008-0011-2
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11099-008-0011-2