Cookies Policy

This site uses cookies. By continuing to browse the site you are agreeing to our use of cookies.

I accept this policy

Find out more here

The kinetic properties of ribulose-1,5-bisphosphate carboxylase/oxygenase may explain the high apparent photosynthetic affinity of Nannochloropsis sp. to ambient inorganic carbon

No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.
The full text of this article is not currently available.

Brill’s MyBook program is exclusively available on BrillOnline Books and Journals. Students and scholars affiliated with an institution that has purchased a Brill E-Book on the BrillOnline platform automatically have access to the MyBook option for the title(s) acquired by the Library. Brill MyBook is a print-on-demand paperback copy which is sold at a favorably uniform low price.

Access this article

+ Tax (if applicable)
Add to Favorites
You must be logged in to use this functionality

image of Israel Journal of Plant Sciences

The marine unicellular alga Nannochloropsis sp. (Eustigmatophyceae) exhibits high apparent affinity for extracellular inorganic carbon (Ci) despite the fact that its ability to accumulate Ci within the cells is relatively low. Kinetic investigation of carboxylation enzyme, ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO), isolated from Nannochloropsis suggests that the latter discrepancy can be accounted for by the high affinity of RubisCO for CO2. A K m(CO2) of 7-10 μM was obtained both by a standard radiolabeling approach and by novel methodology using membrane inlet mass spectrometry. The latter allows precise determination of the changes in the concentrations of dissolved CO2 and O2 as the reaction proceeds. The kinetic parameters of the oxygenase reaction, deduced from measurements of oxygen level, indicated a high K m(O2) (about 1 mM) and high V max (3.9 μmol O2 min-1 mg-1 protein) values, compared to those observed in green algae. Thus, despite Nannochloropsis RubisCO's low K m(CO2), an unusually low specificity factor of 27 was calculated, lower than observed in cyanobacteria and close to values found in anaerobic organisms. We proposed that the elevated CO2 level within the cells, indicated by massive net efflux of CO2 during steady state photosynthesis, is essential for its growth under the high O2 concentrations prevailing in the environment.

Affiliations: 1: Department of Evolution, Systematics and Ecology, The Hebrew University of Jerusalem ; 2: The Interuniversity Institute for Marine Science ; 3: The Yigal Allon Kinneret Limnological Laboratory, Israel Oceanographic and Limnological Research ; 4: Department of Plant Sciences and the Minerva Center for Photosynthesis Under Stress, The Hebrew University of Jerusalem ; 5: The Yigal Allon Kinneret Limnological Laboratory, Israel Oceanographic and Limnological Research


Full text loading...


Data & Media loading...

1. Andrews, T. J., Lorimer, G. H. 1987. RubisCO: structure, mechanism and prospects for improvement. In: Hatch, M. D., Boardman, N. K., eds. Photosynthesis. Academic Press, pp. 131-218.
2. Badger, M. R., Spalding, M. H. 2000. CO2 acquisition, concentration and fixation in cyanobacteria and algae. In: Leegood, R. C., Sharkey, T. D., von Caemmerer, S., eds. Photosynthesis: physiology and metabolism. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 369-397.
3. Badger, M. R., Kaplan, A., Berry, J. A. 1980. The internal inorganic carbon pool of Chlamydomonas reinhardtii: Evidence for a CO2 concentrating mechanism. Plant Physiol. 66: 407-413.
4. Badger, M. R., Andrews, T. J., Whitney, S. M., Ludwig, M., Yellowlees, D. C., Leggat, W., Price, G. D. 1998. The diversity and co-evolution of Rubisco, plastids, pyrenoids and chloroplast-based CCMs in the algae. Can. J. Bot. 76: 1052-1071.
5. Bainbridge, G., Madgwick, P., Parmar, S., Mitchell, R., Paul, M., Pitts, J., Keys, A. J., Parry, M. A. J. 2000. Engineering Rubisco to change its catalytic properties. J. Exp. Bot. 46: 1269-1276.
6. Chen, Z., Spreitzer, R. J. 1989. Nuclear mutation affecting rubisco CO2/O2 specificity. Plant Physiol. Suppl. Abstract #465.
7. Edmondson, D. L., Badger, M. R., Andrews, T. J. 1990. Slow inactivation of ribulosebisphosphate carboxylase during catalysis is caused by accumulation of a slow, tight-binding inhibitor at the catalytic site. Plant Physiol. 93: 1390-1397.
8. Espie, G. S., Kandasamy, R. A. 1994. Monensin inhibition of Na+-dependent HCO3--transport distinguishes it from Na+-independent HCO3- transport and provides evidence for Na+/HCO3- symport in the cyanobacterium Synechococcus UTEX 625. Plant Physiol. 104: 1419-1428.
9. Galmés, J., Flexas, J., Keys, A. J., Cifre, J., Mitchell, R. A. C., Madgwick, P. J., Haslam, R. P., Medrano, H., Parry, M. A. J. 2005. Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant Cell Environ. 28: 571-579.
10. Galmés, J., Medrano, H., Flexas, J. 2006. Acclimation of Rubisco specificity factor to drought in tobacco: discrepancies between in vitro and in vivo estimations. J. Exp. Bot. 57: 3659-3667.
11. Ghoshal, D., Goyal, A. 2000. Carbon concentration mechanisms in photosynthetic microorganisms. Indian J. Biochem. Biophy. 37: 383-394.
12. Hassidim, M., Keren, N., Ohad, I., Reinhold, L., Kaplan, A. 1997. Acclimation of Synechococcus strain WH7803 to ambient CO2 concentration and to elevated light intensity. J. Phycol. 33: 811-817.
13. Huertas, I. E., Espie, G. S., Colman, B., Lubian, L. M. 2000. Light-dependent bicarbonate uptake and CO2 efflux in the marine microalga Nannochloropsis gaditana.Planta 211: 43-49.
14. Huertas, I. E., Colman, B., Espie, G. S. 2002. Inorganic carbon acquisition and its energization in eustigmatophyte algae. Funct. Plant Biol. 29: 271-277.
15. Johnson, K. S. 1982. Carbon dioxide hydration and dehydration in sea water. Limnol. Oceanogr. 27: 849-855.
16. Jordan, D. B., Ogren, W. L. 1981. Species variation in the specificity of ribulose bisphosphate carboxylase/oxygenase. Nature 219: 513-515.
17. Kane, H. J., Viil, J., Entsch, B., Paul, J. H., Morell, M. K., Andrews, T. J. 1994. An improved method for measuring the CO2/O2 specificity of ribulose bisphosphate carboxylase-oxygenase. Aust. J. Plant Physiol. 21: 449-461.
18. Kaplan, A., Reinhold, L. 1999. The CO2 concentrating mechanisms in photosynthetic microorganisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 539-570.
19. Kaplan, A., Badger, M. R., Berry, J. A. 1980. Photosynthesis and intracellular inorganic carbon pool in the blue-green algae Anabaena variabilis: Response to external CO2 concentration. Planta 149: 219-226.
20. Laing, W. A., Ogren, W. E., Hageman, R. H. 1974. Regulation of soybean net photosynthetic CO2 fixation by the interation of CO2 and O2 and ribulose 1,5-diphosphate carboxylase. Plant Physiol. 54: 678-685.
21. Li, G., Mao, H., Ruan, X., Xu, Q., Gong, Y., Zhang, X., Zhao, N. 2003. An improved equation and assay for determining the CO2/O2 specificity for Rubisco. Photosynth. Res. 75: 287-292.
22. Moroney, J. V., Somanchi, A. 1999. How do algae concentrate CO2 to increase the efficiency of photosynthetic carbon fixation? Plant Physiol. 119: 9-16.
23. Ohkawa, H., Sonoda, M., Hagino, N., Shibata, M., Pakrasi, H. B., Ogawa, T. 2002. Functionally distinct NAD(P)H dehydrogenases and their membrane localization in Synechocystis sp PCC6803. Funct. Plant Biol. 29: 195-200.
24. Parry, M. A. J., Keys, A. J., Gutteridge, S. 1989. Variation in the specificity factor of C3 higher plant Rubiscos determined by the total consumption of ribulose-P. J. Exp. Bot. 40: 317-320.
25. Pierce, J. 1989. Rubisco: Mechanisms and their possible constrains on substrate specificity. In: Briggs, W. R., ed. Photosynthesis. Alan R. Liss Inc., New York, pp. 149-159.
26. Portis, A. R. Jr. 1995. The regulation of Rubisco by Rubisco activase. J. Exp. Bot. 46: 1285-1291.
27. Price, G. D., Badger, M. R., Woodger, F. J., Long, B. M. 2008. Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J. Exp. Bot. 59: 1441-1461.
28. Raven, J. A. 1997. Inorganic carbon acquisition by marine autotrophs. Adv. Bot. Res. 27: 85-209.
29. Shibata, M., Ohkawa, H., Kaneko, T., Fukuzawa, H., Tabata, S. and Kaplan, A. 2001. Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: novel genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc. Natl. Acad. Sci. USA 98: 11789-11794.
30. Spalding, M. H., Portis, A. R. 1985. A model for carbon dioxide assimilation in Chlamydomonas reinhardtii.Planta 164: 308-320.
31. Spreitzer, R. J. 1999. Questions about the complexity of chloroplast ribulose-1,5- bisphosphate carboxylase/oxygenase. Photosynth. Res. 60: 29-42.
32. Spreitzer, R. J., Salvucci, M. E. 2002. RubisCO: structure, regulatory interactions, and possibilities for a better enzyme. Annu. Rev. Plant Biol. 53: 449-475.
33. Sukenik, A., Livne, A., Neori, A., Yacobi, Y. Z., Katcoff, D. 1992. Purification and characterization of a light-harvesting chlorophyll-protein complex from the marine eustigmatophyte Nannochloropsis sp. Plant Cell Physiol. 33: 1041-1048.
34. Sukenik, A., Yamaguchi, Y., Livne, A. 1993. Alterations in lipid molecular-species of the marine eustigmatophyte Nannochloropsis sp. J. Phycol. 29: 620-626.
35. Sukenik, A., Tchernov, D., Huerta, E., Lubian, L. M., Kaplan, A., Livne, A. 1997. Uptake, efflux and photosynthetic utilization of inorganic carbon by the marine eustigmatophyte Nannochloropsis sp. J. Phycol. 33: 969-974.
36. Sulpice, R., Tschoep, H., Von Korff, M., Büssis, D., Usadel, B., Höhne, M., Witucka-Wall, H., Altmann, T., Stitt, M., Gibon, Y. 2007. Description and applications of a rapid and sensitive non-radioactive microplate-based assay for maximum and initial activity of D-ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Cell Environ. 30: 1163-1175.
37. Sultemeyer, D., Klughammer, B., Badger, M. R., Price, G. D. 1998. Fast induction of high-affinity HCO3- transport in cyanobacteria. Plant Physiol. 116: 183-192.
38. Tabita, F. R. 1999. Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: a different perspective. Photosynth. Res. 60: 1-28.
39. Tchernov, D., Hassidim, M., Luz, B., Sukenik, A., Reinhold, L., Kaplan, A. 1997. Sustained net CO2 evolution during photosynthesis by marine microorganisms. Curr. Biol. 7: 723-728.
40. Tchernov, D., Helman, Y., Keren, N., Luz, B., Ohad, I., Reinhold, L., Ogawa, T., Kaplan, A. 2001. Passive entry of CO2 and its energy-dependent intracellular conversion to HCO3- in cyanobacteria are driven by a photosystem I-generated ΔμH+. J. Biol. Chem. 276: 23450-23455.
41. Tu, C. K., Spiller, H., Wynns, G. C., Silverman, D. N. 1987. Carbonic anhydrase and the uptake of inorganic carbon by Synechococcus sp. (UTEX 2380). Plant Physiol. 85: 72-77.
42. Uemura, K., Suzuki, Y., Shikanai, T., Wadano, A., Jensen, R. G., Chmara, W., Yokota, A. 1996. A rapid and sensitive method for determination of relative specificity of RuBisCO from various species by anion-exchange chromatography. Plant Cell Physiol. 37: 325-331.
43. Whitney, S. M., Andrews, T. J. 1998. The CO2/O2 specificity of single-subunit ribulose-bisphosphate carboxylase from the dinoflagellate, Amphidinium carterae.Aust. J. Plant Physiol. 25: 131-138.

Article metrics loading...



Can't access your account?
  • Tools

  • Add to Favorites
  • Printable version
  • Email this page
  • Subscribe to ToC alert
  • Get permissions
  • Recommend to your library

    You must fill out fields marked with: *

    Librarian details
    Your details
    Why are you recommending this title?
    Select reason:
    Israel Journal of Plant Sciences — Recommend this title to your library
  • Export citations
  • Key

  • Full access
  • Open Access
  • Partial/No accessInformation