Skip to main content
SpringerLink
Log in

Photosystem II photoinhibition and altered kinetics of photosynthesis during nutrient-dependent high-light photoadaptation in Gonyaulax polyedra

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Gonyaulax poledra Stein was transferred at different cell densities from increasingly nutrient-limited low-light (LL, 80 μE m-2 s-1) batch-cultures to high-light (HL, 330 μE m-2 s-1) growth conditions. Several age-dependent differences in HL-adaptation strategies were apparent. Short-term (≦3h) susceptibility to photosynthetic photoinhibition increased with culture age, with light-limited rates of photosynthesis exhibiting greater photosuppression than light-saturated rates at all stages of growth. These shortterm changes were not accompanied by photobleaching of chlorophyll but were directly related to age-dependent photoinactivation of Photosystem II electron-transport rates. The capacity of electron transport by Photosystem I was only slightly affected. Prolonged exposure of LL log-phase cells to HL conditions did induce photobleaching of chlorophyll associated with increased cell volume, a transient decrease of organic carbon and nitrogen content, enhanced cellular-, carbon-and chlorophyll-based rates of light-saturated photosynthesis (P max) and suppressed cellular rates of light-limited photosynthesis. As a result, the density of LL log-phase cells doubled and their cellular photosynthetic performance nearly tripled within 1 d of HL exposure while cellular respiratory demands remained unchanged. By contrast, prolonged HL incubation of LL stationary populations induced a transitory burst in cell division and a large reduction in cell volume, leading to a short-term increase in volume-based organic carbon and nitrogen content. Despite reduced cell volume and lowered carbon demand, the cellular-, carbon-and chlorophyll-based rates of P max in nondividing populations fell by 64, 48 and 27%, respectively, over a 4 d exposure to HL, while light-limited rates were almost fully suppressed within 1 d and chlorophyll a content was reduced by 56%. As a result, the photosynthetic performance of LL-aged cells declined immediately under HL conditions. Addition of inorganic nutrients to LL stationary cultures at the time of HL transfer led to immediate and complete suppression of photosynthesis and cell lysis within 1 d. Addition of nutrients following transfer to HL induced cell responses intermediate to those described for LL log and aged cells exposed to HL. Results support the view that declining nutrient-status impairs HL photoadaptive responses in phytoplankton populations and that the rate and pattern of photoadaptive responses may be used as physiological growth indicators in field studies. The study was conducted from March 1981 to May 1983.

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

  • Bjorkman, O.: Responses to different quantum flux densities. In: Encyclopedia of plant physiology, pp 57–107. Ed. by O. L. Lange, P. S. Nobel, C. B. Osmond and H. Ziegler. Berlin: Springer-Verlag 1981

    Google Scholar 

  • Boczar, B. A. and B. B. Prézelin: Light and MgCl2-dependent characteristics of four chlorophyll-protein complexes from the marine dinoflagellate, Glenodinium sp. Biochim. biophys. Acta (In press). (1986)

  • Boczar, B. A. and B. B. Prézelin: Light-dependent chlorophyllprotein organization within the photosynthetic apparatus of the red-tide dinoflagellate Gonyaulax polyedra Stein (In preparation)

  • Boczar, B. A., B. B. Prézelin, J. P. Markwell and J. P. Thornber: A chlorophyll c-containing pigment-protein complex from the marine dinoflagellate, Glenodinium sp. Fedn eur. biochem. Soc. (FEBS) Lett. 120, 243–247 (1980)

    Google Scholar 

  • Brooks, J. E.: Acclimation to light intensity in two species of marine phytoplankton, Dunaliella tertiolecta Butcher and Skeletonema (Greve) Cleve, 30 pp. M.S. thesis, University of Southern California 1964

  • Falkowski, P. G.: Kinetics of adaptation to irradiance in Dunaliella tertiolecta. Photosynthetica (Praha, Czechoslovakia) 18, 62–68 (1984)

    Google Scholar 

  • Falkowski, P. G. and D. P. Stone: Nitrate uptake in marine phytoplankton: energy sources and the interaction with carbon fixation. Mar. Biol. 32, 77–84 (1975)

    Google Scholar 

  • Gattuso, J.-P. and J. Jaubert: Preliminary data concerning the in situ effects of light on metabolism, growth and calcification of the hermatypic coral Stylophora pistillata. C. r. hebd. Séanc. Acad. Sci., Paris 299, 585–590 (1984)

    Google Scholar 

  • Govindjee, D. Wong, B. B. Prézelin and B. M. Sweeney: Chlorophyll a fluorescence of Gonyaulax polyedra grown on a light-dark cycle and after transfer to constant light. Photochem. Photobiol. 30, 405–411 (1979)

    Google Scholar 

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

    Google Scholar 

  • Harding, L. W. Jr., B. W. Meeson, B. B. Prézelin and B. M. Sweeney: Diel periodicity of photosynthesis in marine phytoplankton. Mar. Biol. 61, 95–105 (1981)

    Google Scholar 

  • Harris, G. P.: Photosynthesis, productivity and growth: the physiological ecology of phytoplankton. Arch. Hydrobiol. (Beih. Ergebn. Limnol.) 10, 1–171 (1978)

    Google Scholar 

  • Jassby, A. D. and T. Platt: Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol. Oceanogr. 21, 540–547 (1976)

    Google Scholar 

  • Krinsky, N. I.: Carotenoid pigments: multiple mechanisms for coping with the stress of photosensitized oxidations. In: Strategies of microbial life in extreme environments, pp 163–187. Ed. by M. Shilo. New York: Gustav Fisher Inc. 1979

    Google Scholar 

  • Kyle, D. J., I. Ohad and C. J. Arntzen: Membrane protein damage and repair: selective loss of a quinone-protein function in chloroplast membranes. Proc. natn. Acad. Sci. U.S.A. 81, 4070–4074 (1984)

    Google Scholar 

  • Ogren, E. and G. Oquist: Photoinhibition of photosynthesis in Lemna gibba as induced by the interaction between light and temperature. II. Photosynthetic electron transport. Physiologia Pl. 62, 187–192 (1984)

    Google Scholar 

  • Ogren, E., G. Oquist and J. E. Hallgren: Photoinhibition of photosynthesis in Lemna gibba as induced by the interaction between light and temperature. I. Photosynthesis in vivo. Physiologia Pl. 62, 181–186 (1984)

    Google Scholar 

  • Ohad, I., D. J. Kyle and C. J. Arntzen: Membrane protein damage and repair: removal and replacement of inactivation 32-kilodalton polypeptides in chloroplast membranes. J. Cell Biol. 99, 481–485 (1984)

    Google Scholar 

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

    Google Scholar 

  • Perry, M. J., M. C. Talbot and R. S. Alberte: Photoadaption in marine phytoplankton: response of the photosynthetic unit. Mar. Biol. 62, 91–101 (1981)

    Google Scholar 

  • Post, A. F., Z. Dubinsky, K. Wyman and P. G. Falkowski: Kinetics of light-intensity adaptation in a marine planktonic diatom. Mar. Biol. 83, 231–238 (1984)

    Google Scholar 

  • Powles, S. B.: Photoinhibition of photosynthesis induced by visible light. A. Rev. Pl. Physiol. 34, 15–44 (1984)

    Google Scholar 

  • Prézelin, B. B.: Light reactions in photosynthesis. Can. Bull. Fish. aquat. Sciences. 210, 1–43 (1981)

    Google Scholar 

  • Prézelin, B. B.: Effects of light intensity on aging of the dinoflagellate Gonyaulax polyedra. Mar. Biol. 69, 129–135 (1982)

    Google Scholar 

  • Prézelin, B. B.: Photosynthetic physiology of dinoflagellates. In: The dinoflagellates, pp 174–223. Ed. by D. J. Taylor. London: 1986

  • Prézelin, B. B. and R. S. Alberte: Photosynthetic characteristics and organization of chlorophyll in marine dinoflagellates. Proc. natn. Acad. Sci. U.S.A. 75, 1801–1804 (1978)

    Google Scholar 

  • Prézelin, B. B. and B. A. Boczar: Molecular bases of cell absorption and fluorescence in phytoplankton: potential applications to studies in optical oceanography. In: Progress in phycological research, Vol. 4. pp 270–386. Ed. by. F. Round and D. Chapman. Bristol: Biopress Ltd. 1986

    Google Scholar 

  • Prézelin, B. B. and F. T. Haxo: Purification and characterization of peridinin-chlorophyll a-proteins isolated from the marine dinoflagellates, Glenodinium sp. and Gonyaulax polyedra. Planta 128, 133–141 (1976)

    Google Scholar 

  • Prézelin, B. B. and H. A. Matlick: Time-course of photoadaptation in the photosynthesis-irradiance relationship of a dinoflagellate exhibiting photosynthetic periodicity. Mar. Biol. 58, 85–96 (1980)

    Google Scholar 

  • Prézelin, B. B. and H. A. Matlick: Nutrient-dependent low-light adaptation in the dinoflagellate Gonyaulax polyedra. Mar. Biol. 74, 141–150 (1983)

    Google Scholar 

  • Prézelin, B. B., B. W. Meeson and B. M. Sweeney: Characterization of photosynthetic rhythms in marine dinoflagellates. I. Pigmentation, photosynthtic capacity and respiration. Pl. Physiol., Baltimore, Md 60, 384–387 (1977)

    Google Scholar 

  • Prézelin, B. B. and B. M. Sweeney: Photoadaptation of photosynthesis in Gonyaulax polyedra. Mar. Biol. 48, 27–35 (1978)

    Google Scholar 

  • Richardson, K., J. Beardall and J. Ravens: Adaptation of unicellular algae to irradiance: an analysis of strategies. New Phytol. 93, 157–191 (1983)

    Google Scholar 

  • Samuelsson, G., A. Lonnborg, E. Rosenqvist, P. Gustavsson and G. Oquist: Photoinhibition and reactivation of photosynthesis in the cyanobacterium Anacystis nidulans. Pl. Physiol. Baltimore, Md 79, 992–995 (1985)

    Google Scholar 

  • Samuelsson, G. and B. B. Prézelin: Photosynthetic electron transport in cell-free extracts of diverse phytoplankton. J. Phycol. 21, 453–457 (1985)

    Google Scholar 

  • Samuelsson, G. and K. Richardson: Photoinhibition at low quantum flux densities in a marine dinoflagellate (Amphidinium carterae). Mar. Biol. 70, 21–26 (1982)

    Google Scholar 

  • Samuelsson, G., B. M. Sweeney, H. A. Matlick and B. B. Prézelin: Changes in photosystem II account for the circadian rhythm in photosynthesis in Gonyaulax polyedra. Pl. Physiol. Baltimore, Md 73, 329–331 (1983)

    Google Scholar 

  • Turpin, D. H.: Ammonium induced photosynthetic suppression in ammonium limited Dunaliella tertiolecta (Chlorophyceae). J. Phycol. 19, 70–76 (1983)

    Google Scholar 

  • Tytler, E. M., G. C. Whitelam, M. F. Hipkins and G. A. Codd: Photoinactivation of photosystem II during photoinhibition in the cyanobacterium Microcystis aeruginosa. Planta 160, 229–234 (1984)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Oceanic Biology Group, Marine Science Institute, 93106, Santa Barbara, California, USA

    B. B. Prézelin & H. A. Matlick

  2. Department of Biological Sciences, University of California at Santa Barbara, 93106, Santa Barbara, California, USA

    B. B. Prézelin & H. A. Matlick

  3. Department of Plant Physiology, University of Umeå, S-90187, Umeå, Sweden

    G. Samuelsson

Authors
  1. B. B. Prézelin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Samuelsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. A. Matlick
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by R. S. Carney, Moss Landing

Rights and permissions

Reprints and permissions

About this article

Cite this article

Prézelin, B.B., Samuelsson, G. & Matlick, H.A. Photosystem II photoinhibition and altered kinetics of photosynthesis during nutrient-dependent high-light photoadaptation in Gonyaulax polyedra . Marine Biology 93, 1–12 (1986). https://doi.org/10.1007/BF00428648

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00428648

Keywords

Search

Navigation