Skip to main content
SpringerLink
Log in

Carbon fixation in marine phytoplankton: carboxylase activities and stable carbon-isotope ratios; physiological and paleoclimatological aspects

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

We measured the activity of three carboxylases: RuBP carboxylase, PEP carboxylase and PEP carboxykinase of marine phytoplankton species in culture and in natural communities. Activities of the three carboxylases were measured simultaneously with stable carbon-isotope ratios. The enzymatic activities have been used to estimate the importance of β carboxylation and its impact on the 13C:12C ratio (expressed as δ13C). The marine phytoplankton species in culture were Fragilariopsis kerguelensis, Nitzschia turgiduloides, Skeletonema costatum, Phaeodactylum tricornutum, Isochrysis galbana, Dunaliella marina, and Prorocentrum micans, and the field samples were collected from different depths off the coast of Portugal (August/September, 1981). Our results indicate that, as in terrestrial plants, the δ13C value is a good indicator of the extent of β carboxylation. RuBP carboxylase activity was always predominant, whereas the δ13C value never reached values typical of the C4 pathway. The β carboxylases could be PEP carboxylase (in dinoflagellates) or PEP carboxykinase (in diatoms). β carboxylation increased at the end of the exponential growth phase in a diatom culture and with increased biomass in natural samples. We interpret these increases as an adaptative response mechanism to poor environmental conditions, especially to low light intensity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature cited

  • Appleby, G., J. Colbeck, E. S. Holdsworth and H. Wadman: β carboxylation enzymes in marine phytoplankton and isolation and purification of pyruvate and carboxylase from Amphidinium carterae (Dinophyceae). J. Phycol. 16, 290–295 (1980)

    Google Scholar 

  • Beardall, J., D. Mukerji, H. E. Glover and I. Morris: The path of carbon in photosynthesis by marine phytoplankton. J. Phycol. 12, 409–417 (1976)

    Google Scholar 

  • Benedict, C. R.: Nature of obligate photoautotrophy. A. Rev. Pl. Physiol. 29, 67–93 (1978)

    Article  Google Scholar 

  • Bradshaw, A. L. and P. G. Brewer: The titration of sea-water with strong acid. Tech. Rep. Woods Hole oceanogr. Instn 1980

  • Chesselet, R., M. R. Fontugne, P. Buat-Menard, U. Ezat and C. E. Lambert. The origin of particulate organic carbon in the marine atmosphere as indicated by its stable carbon isotopic composition. Geophys. Res. Lett. 8, 345–348 (1981)

    Google Scholar 

  • Descolas-Gros, C.: Les voies d'incorporation photosynthétique du carbone du phytoplancton. Signification écologique de l'activité des carboxylases en milieu marin. Comparaison avec le rapport isotopique 13C:12C du carbone organique du phytoplancton, 117 pp. Thèse Doctorat ès Sciences, Paris VI, 1983

  • Dyrssen, D. and C. G. Sillen: Alkalinity and total carbonate in sea-water; a plea for P. T. independent data. Tellus 19, 113–121 (1967)

    Google Scholar 

  • Brunet, C. et A. Poisson: Alcalinité totale-carbone inorganique total. Densité. Publs Cent. natn. Exploit. Océans (CNEXO) 25, 49–51 (1983)

    Google Scholar 

  • Edmond, J. M.: High precision determination of titration alkalinity and total CO2 of sea-water by potentiometric titration. Deep-Sea Res. 17, 737–750 (1970)

    Google Scholar 

  • Fontugne, M. R.: Les isotopes stables du carbone organique dans l'océan. Applications à la paléoclimatologie, 228 pp. Thèse Doctorat ès Sciences, Orsay 1983

  • Fontugne, M. R. and J. C. Duplessy: Carbon isotope ratio of marine plankton related to surface water masses. Earth planet. Sci. Lett. 41, 365–371 (1978)

    Article  Google Scholar 

  • Fontugne, M. R. and J. C. Duplessy: Organic isotopic fractionation by marine plankton in the temperature range-1 to 31°C. Oceanol. Acta 4, 85–90 (1981)

    Google Scholar 

  • Gifford, R. M.: A comparison of potential photosynthesis productivity and yield of plant species with differing photosynthetic metabolism. Aust. J. Pl. Physiol. 1, 107–117 (1974)

    Google Scholar 

  • Gross, F.: Notes on the culture of some marine plankton organisms. J. mar. biol. Ass. U.K. 21, 753–768 (1937)

    Google Scholar 

  • Guillard, R. R. L. and J. H. Ryther: Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8, 229–239 (1962)

    PubMed  Google Scholar 

  • Holdsworth, E. S. and J. Colbeck: The pattern of carbon fixation in the marine unicellular alga Phaeodactylum tricornutum. Mar. Biol. 38, 189–199 (1976)

    Google Scholar 

  • Holdsworth, E. S. and K. Bruck: Enzymes concerned with β carboxylation in marine phytoplankter purification and properties of phosphoenopyruvate carboxykinase. Archs Biochem. Biophys. 182, 87–94 (1977)

    Google Scholar 

  • Holm-Hansen, O., C. J. Lorenzen, R. W. Holmes and J. D. H. Strickland: Fluorometric determination of chlorophyll. J. Cons. perm. int. Explor. Mer 30, 3–15 (1965)

    Google Scholar 

  • Jolivet, E.: Les différentes modalités de carboxylation photosynthétique chez les espèces de type C3 et de type C4. Physiologie vég. 14, 563–594 (1976)

    Google Scholar 

  • Kaplan, A., M. R. Badger and J. A. Berry: Photosynthesis and the intracellular inorganic carbon pool in the blue-green alga Anabaena variabilis: response to external CO2 concentration. Planta 149, 219–226 (1980)

    Google Scholar 

  • Kelly, G. J. and E. Latzko: Regulatory aspects of photosynthetic carbon metabolism. A. Rev. Pl. Physiol. 27, 181–205 (1976)

    Article  Google Scholar 

  • Kremer, B. P. and R. Berks: Photosynthesis and carbon metabolism in marine and freshwater diatoms. Z. PflPhysiol. 87, 149–165 (1978)

    Google Scholar 

  • Lavergne, D., E. Bismuth and M. L. Champigny: Physiological studies on two cultivars of Pennisetum: P. americanum 23DB, a cultivated species and P. mollissimum, a wild species. I. Photosynthetic carbon metabolism. Z. PflPhysiol., 91, 291–303 (1979a)

    Google Scholar 

  • Lavergne, D., E. Bismuth, E. Sarda and M. L. Champigny: Physiological studies on two cultivars, of Pennisetum: P. americanum 23 DB, a cultivated species and P. mollissimum, a wild species. II. Effects of leaf age on biochemical characteristics and activities of the enzymes associated with the photosynthetic carbon metabolism. Z. PflPhysiol. 93, 159–170 (1979b)

    Google Scholar 

  • Li, W. K. W., H. E. Glover and I. Morris: Physiology of carbon photoassimilation by Oscillatoria thiebautii in the Caribbean sea. Limnol. Oceanogr. 25, 447–456 (1980)

    Google Scholar 

  • Médiprod Groupe. Remontées d'eaux sur les côtes atlantiques du Portugal. Campagne RCA I. (28 août-19 septembre 1981). Publs Cent. natn. Exploit. Océans (CNEXO) (Sér. Résult. Campagnes Mer) 25, 1–115 (1983)

    Google Scholar 

  • Miller, A. G. and B. Colman: Evidence for -3 transport by the blue green alga (cyanobacterium) Coccochloris peniocystis. Plant Physiol., Lancaster, Pa. 65, 397–402 (1980)

    Google Scholar 

  • Morris, I.: Paths of carbon assimilation in marine phytoplankton. In: Primary productivity in the sea, pp 139–159. Ed. by P. G. Falkowski. New York: Plenum Press 1980

    Google Scholar 

  • Morris, I., A. E. Smith and H. E. Glover: Products of photosynthesis in phytoplankton off the Orinoco river and in the Caribbean Sea. Limnol. Oceanogr. 26, 1034–1044 (1981)

    Google Scholar 

  • Moyse, A.: Les types métaboliques des plantes C4 et CAM. Comparaison avec les plantes C3. Physiologie vég. 14, 533–550 (1976)

    Google Scholar 

  • Mukerji, D. and I. Morris: Photosynthetic carboxylating enzymes in Phaeodactylum tricornutum: assay methods and properties. Mar. Biol. 36, 199–206 (1976)

    Google Scholar 

  • Osmond, C. B.: Photorespiration and photoinhibition. Some implications for the energetics of photosynthesis. Biochim. biophys. Acta 639, 77–98 (1981)

    Google Scholar 

  • Platt, T., D. V. Subba Rao, J. C. Smith, W. K. Li, B. Irwin, E. P. W. Horne and D. D. Sameoto: Photosynthetically competent phytoplankton from the aphotic zone of the deep ocean Mar. Ecol. Prog. Ser. 10, 105–110 (1983)

    Google Scholar 

  • Rau, G. H., R. E. Sweeney and I. R. Kaplan: Plankton 13C:12C ratio changes with latitude: differences between northern and southern oceans. Deep-Sea Res. 29, 1035–1039 (1982)

    Article  Google Scholar 

  • Sackett, W. M., B. J. Eadie and M. E. Exner: Stable isotope composition of organic carbon in recent Antarctic sediments In: Advances in organic chemistry, pp 661–671. Ed. by B. Tissot and F. Bienner. Paris: Technip 1974. (Procès 6ème congrès international de géochimie organique, Rueil Malmaison, France, 1973)

    Google Scholar 

  • Sackett, W. M., W. R. Eckelmann, M. L. Bender and A. W. H. Be: Temperature dependence of carbon isotopes in marine plankton and sediments. Science, N.Y. 148, p. 235 (1965)

    Google Scholar 

  • Smith, J. C., T. Platt and W. G. Harrison: Photoadaptation of carboxylating enzymes and photosynthesis during a spring bloom. Prog. Oceanogr. 12 425–459 (1983)

    Article  Google Scholar 

  • Troughton, J.H.: ¢13C as an indicator of carboxylation reactions. In: Encyclopedia of plant physiology, photosynthesis II Vol. 6. pp 140–147. Ed. by M. Gibbs and E. Latzko. Berlin: Springer-Verlag 1979

    Google Scholar 

  • Wong, W. W. L.: Carbon isotope fractionation by marine phytoplankton, 116 pp. PhD thesis, Texas A&M University 1976

Download references

Author information

Authors and Affiliations

  1. Laboratoire Arago, Université Pierre et Marie Curie, F-66650, Banyuls-sur-Mer, France

    C. Descolas-Gros

  2. Centre des Faibles Radioactiviés, Laboratoire Mixte CEA-CNRS, B.P. 1, F-91190, Gif-sur-Yvette, France

    M. R. Fontugne

Authors
  1. C. Descolas-Gros
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. R. Fontugne
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by J. M. Pérès, Marseille

Rights and permissions

Reprints and permissions

About this article

Cite this article

Descolas-Gros, C., Fontugne, M.R. Carbon fixation in marine phytoplankton: carboxylase activities and stable carbon-isotope ratios; physiological and paleoclimatological aspects. Marine Biology 87, 1–6 (1985). https://doi.org/10.1007/BF00396999

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00396999

Keywords

Search

Navigation