Abstract
A mutant of the cyanobacterium Synechocystis PCC 6803 was obtained by replacing the gene of the carboxylation enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) with that of the photosynthetic bacterium Rhodospirillum rubrum. This mutant consequently lacks carboxysomes — the protein complexes in which the original enzyme is packed. It is incapable of growing at atmospheric CO2 levels and has an apparent photosynthetic affinity for inorganic carbon (Ci) which is 1000 times lower than that of the wild type, yet it accumulates more Ci than the wild type. The mutant appears to be defective in its ability to utilize the intracellular Ci pool for photosynthesis. Unlike the carboxysomal carboxylase activity of Rubisco, which is almost insensitive to inhibition by O2 in vitro, the soluble enzyme is competitively inhibited by O2. The photosynthetic rate and Ci compensation point of the wild type were hardly affected by low O2 levels. Above 100 μM O2, however, both parameters became inhibited. The CO2 compensation point of the mutant was linearly dependent on O2 concentration. The higher sensitivity of the mutant to O2 inhibition than that expected from in-vitro kinetics parameters of Rubisco, indicates a low capacity to recycle photorespiratory metabolites to Calvin-cycle intermediates.
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Abbreviations
- ci :
-
inorganic carbon
- RuBP:
-
ribulose-1,5-bisphosphate
- Rubisco:
-
ribulose-1,5-bisphosphate carboxylase/oxygenase
References
Badger, M.R. (1987) The CO2 concentrating mechanism in aquatic phototrophs. In: The biochemistry of plants, vol. 10, pp. 219–273, Hatch, H.D., Boardman, N.R., eds. Academic Press, San Diego
Badger, M.R., Andrews, T.J. (1987) Co-evolution of Rubisco and CO2 concentrating mechanisms. Progr. Photosynth. Res. 9, 601–609
Badger, M.R., Bassett, M., Comins, H.N. (1985) A model for HCO −3 accumulation and photosynthesis in the cyanobacterium Synechococcus sp.: Theoretical prediction and experimental observation. Plant Physiol. 77, 465–471
Chastain, C.J., Ogren, W.L. (1985) Photorespiration induced reduction of ribulose bisphosphate carboxylase activation level. Plant Physiol. 77, 851–856
Codd, G.A., Marsden, W.J.N. (1984) The carboxysomes (polyhedral bodies) of autotrophic prokaryotes. Biol. Rev. 59, 389–422
Codd, G.A., Stewart, W.D.P. (1973) Pathways of glycolate metabolism in the blue green alga Anabaena cylindrica. Arch. Microbiol. 94, 11–28
Coleman, J.R., Seeman, J.R., Berry, J.A. (1982) RuBPcarboxylase in carboxysomes of the blue green algae. Carnegie Inst. Washington Yearb. 81, 83–87
Friedberg, D., Kaplan, A., Ariel, R., Kessel M., Seijffers, J. (1989) The 5′ flanking region of the gene encoding the large subunit of Ribulose 1,5 bisphosphate carboxylase/oxygenase is crucial for growth of the cyanobacterium Synechococcus sp. strain PCC 7942 at the level of CO2 in air. J. Bacteriol. 171, 6069–6076
Jordan, D.B., Ogren, W.L. (1981) Species variation in the specificity of ribulose bisphosphate carboxylase/oxygenase. Nature 291, 513–515
Kaplan, A., Berry, J.A. (1981) Glycolate excretion and the oxygen to carbon dioxide net exchange ratio during photosynthesis in Chlamydomonas reinhardtii. Plant Physiol. 67, 229–232
Kaplan, A., Badger, M.R., Berry, J.A. (1980) Photosynthesis and the intracellular inorganic carbon pool in the blue green alga Anabaena variabilis: response to external CO2 concentration. Planta 149, 219–226
Kaplan, A., Marcus, Y., Reinhold, L. (1988) Inorganic carbon uptake by cyanobacteria. Methods Enzymol. 167, 534–538
Kornberg, H.L., Gotto, A.M. (1961) The metabolism of C2 compounds in microorganismes. Synthesis of cell constituents from glycolate by Pseudomonas sp. Biochem. J. 78, 69–81
Marcus, Y., Zenvirth, D., Harel, E., Kaplan, A. (1982) Induction of HCO −3 transporting capability and high photosynthetic affinity in inorganic carbon by low concentration of CO2 in Anabaena variabilis. Plant Physiol. 69, 1008–1012
Marcus, Y., Harel, E., Kaplan, A. (1983) Adaptation of the cyanobacterium Anabaena variabilis to low CO2 concentration in their environment. Plant Physiol. 71, 208–210
Marcus, Y., Schwarz, R., Friedberg, D., Kaplan, A. (1986) High CO2 requiring mutant of Anacystis nidulans R2. Plant Physiol. 82, 610–612
Pearce, J., Leach, C.K., Carr, N.G. (1969) The incomplete tricarboxylic acid cycle in the blue green alga Anabaena variabilis. J. Gen. Microbiol. 55, 371–378
Pierce, J., Carlson, T.J., Williams, J.G.K. (1989) A cyanobacterial mutant requiring the expression of ribulose bisphosphate carboxylase from photosynthetic anaerobe. Proc. Natl. Acad. Sci. USA 86, 5753–5757
Price, G.D., Badger, M.R. (1989) Expression of human carbonic anhydrase in the cyanobacterium Synechococcus PCC 7942 creates a high CO2 requiring mutant phenotype. Plant Physiol. 91, 505–513
Raven, J. (1970) Exogenous inorganic sources in plant photosynthesis. Biol. Rev. 45, 167–221
Reinhold, L., Zviman, M., Kaplan, A. (1987) Inorganic carbon fluxes and photosynthesis in cyanobacteria: a quantitative model. Progr. Photosynth. Res. 6, 289–300
Scherer, S., Almon, H., Boger, P. (1988) Interaction of photosynthesis, respiration and nitrogen fixation in cyanobacteria. Photosynthesis Res. 15, 95–114
Somerville, C.R., Portis, A.R., Ogren, W.L. (1982) A mutant of Arabidopsis thaliana which lacks activation of RuBP carboxylase in vivo. Plant Physiol. 70, 381–387
Stanier, R.Y., Kunisawa, K., Mandel, M., Cohen Bazir, G. (1971) Purification and properties of unicellular blue green algae (order Chroococales). Bacteriol. Rev. 35, 171–205
Tolbert, N.E., Husig, D.H., Husig, D.W., Moroney, J.M., Wilson, B.J. (1985) Relation of glycolate excretion to the DIC pool in microalgae. In: Inorganic carbon uptake by aquatic photosynthetic organisms, pp. 211–227, Lucas, W.L., Berry, J.A., eds. American Society of Plant Physiologists, Rockville
Woodrow, I.E., Berry, J.A. (1988) Enzymatic regulation of photosynthetic CO2 fixation in C3 plants. Annu. Rev. Plant Physiol. 39, 533–593
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Yehouda Marcus was supported by a United States-Israel Binational Agricultural Research and Development Fund (BARD) postdoctoral fellowship and, during the writing of this manuscript, by the Alexander von Humboldt foundation and the Otto Warburg Center for Biotechnology in Agriculture. We thank Professor Nora Reinhold and Professor Aaron Kaplan (Department of Botany, The Hebrew University of Jerusalem, Israel), and Dr. Wil Terazaghi (Department of Plant Biology, Stanford, Calif., USA) for many exciting discussions. We also thank Mrs. Camille Vainstein for her help in preparing the manuscript.
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Marcus, Y., Berry, J.A. & Pierce, J. Photosynthesis and photorespiration in a mutant of the cyanobacterium Synechocystis PCC 6803 lacking carboxysomes. Planta 187, 511–516 (1992). https://doi.org/10.1007/BF00199970
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DOI: https://doi.org/10.1007/BF00199970