Skip to main content
SpringerLink
Log in

Interplay between photochemical activities and pigment composition in an outdoor culture of Haematococcus pluvialis during the shift from the green to red stage

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The transfer of laboratory cultures of H. pluvialis to high irradiance outdoors caused a substantial decline in the maximum quantum yield of photosystem II (PSII), from 0.65 in the morning to 0.45 at midday, as measured by the ratio of variable to maximum fluorescence yields (Fv/Fm), and a steep rise in non-photochemical quenching (NPQ). Chlorophyll fluorescence induction curves of morning samples showed a clear I-step, reflecting a certain PSII heterogeneity. Single turnover flash measurements on samples taken from the outdoor photobioreactor in the middle of day showed an increase in the reoxidation time constant of the reduced plastoquinone QA −, i.e., the time required for electron transfer from the primary plastoquinone acceptor of PSII QA − to the secondary plastoquinone acceptor QB. Photosynthesis rates were almost constant during the day. Along with the increase in non-photochemical quenching, there was a slight increase in zeaxanthin and antheraxanthin contents and decrease in violaxanthin, showing the presence of an operative xanthophyll cycle in this microalga. A marked increase of secondary carotenoids was found at the end of the first day of exposure to sunlight, mainly astaxanthin monoester, which reached 15.5% of the total carotenoid content. Though cells turned reddish during the second day, the decline in the fluorescence parameter Fv/Fm in the middle of the day was less than during the first day, and there was no further increase in the value for NPQ. Similar behaviour was observed during the third day when the culture was fully red. After four days of exposure to sunlight, the dry weight reached 800 mg L−1 and the concentration of secondary carotenoids (81% astaxanthin monoester) reached 4.4% dry weight.

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

References

  • Ben-Amotz A., Shaish A. and Avron M. 1989. Mode of action of the massively accumulated β-carotene of Dunaliella bardawil in protecting the alga against damage by excess irradiation. Plant Physiol. 91: 1040-1043.

    Google Scholar 

  • Bidigare R.G., Ondrusek M.E., Kennicutt M.C. II, Iturriaga R., Harvey H.R., Hoham R.W. et al. 1993. Evidence for a photoprotective function for secondary carotenoids of snow algae. J. Phycol. 29: 427-434.

    Google Scholar 

  • Bilger W. and Björkman O. 1990. Role of xanthophyll in photoprotection elucidated by measurement of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth. Res. 25: 173-185.

    Google Scholar 

  • Bocci F., Torzillo G., Vincenzini M. and Materassi R. 1987. Growth physiology of Spirulina platensis in tubular photobioreactor under sunlight. In: Stadler T., Mollion J., Verdus M.C., Karamanos Y., Morvan H. and Christiaen D. (eds), Algal Biotechnology. Elsevier Applied Sciences Publishers, London, pp. 219-228.

    Google Scholar 

  • Borowitzka M.A., Huisman J.M. and Ann O. 1991. Cultures of theastaxanthin producing green alga Haematococcus pluvialis. 1. Effect of nutrients on growth and cell type. J. appl. Phycol. 3: 295-304.

    Google Scholar 

  • Boussiba S. 2000. Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol. Plant 108: 111-117.

    Google Scholar 

  • Boussiba S., Lu F. and Vonshak A. 1991. Astaxanthin accumulation in the green alga Haematococcus pluvialis. Plant Cell Physiol. 32: 1077-1082.

    Google Scholar 

  • Boussiba S., Lu F. and Vonshak A. 1992. Enhancement and determination of astaxanthin accumulation in green alga Haematococcus pluvialis. Methods Enzymol. 213: 386-391.

    Google Scholar 

  • Demmig-Adams B. 1990. Carotenoids and photoprotection in plants. A role for the xanthophyll zeaxanthin. Biochim. biophys. Acta 1020: 1-24.

    Google Scholar 

  • Diner B.A. 1998. Photosynthesis: Molecular Biology of Energy Capture. Methods Enzymol. 297: 337-360.

    Google Scholar 

  • Gilmore A.M. and Yamamoto H.Y. 1991. Zeaxanthin formation and energy dependent fluorescence quenching in pea chloroplasts under artificially mediated linear and cyclic electron transport. Plant Physiol. 96: 635-643.

    Google Scholar 

  • Govindjee 1995. Sixty-three years since Kautsky: chlorophyll a fluorescence. Austr. J. Plant Physiol. 22: 131-160.

    Google Scholar 

  • Hanagata N. and Dubinsky Z. 1999. Secondary carotenoid accumulation in Scenedesmus komarekii (Chlorophyceae, Chlorophyta). J. Phycol. 35: 960-966.

    Google Scholar 

  • Hagen C., Braune W. and Björn L.O. 1994. Functional aspects ofsecondary carotenoids in Haematococcus lacustris (Girod) Rostafinski (Volvocales). III. Action of a ''sunshade". J. Phycol. 30: 241-248.

    Google Scholar 

  • Lavorel J. and Etienne A.L. 1977. In vivo chlorophyll fluorescence. In: Barber J. (ed.), Primary Processes of Photosynthesis. Elsevier, Amsterdam, pp. 203-268.

    Google Scholar 

  • Lee Y.K. and Soh C.W. 1991. Accumulation of astaxanthin in Haematococcus lacustris (Chlorophyta). J. Phycol. 27: 575-577.

    Google Scholar 

  • Lichtenthaler H.K. 1987. Chlorophylls and carotenoids: pigmentsof photosynthetic membranes. Methods Enzymol. 148: 349-382.

    Google Scholar 

  • Lu K. and Vonshak A. 1999. Characterization of PSII photochemistry in salt-adapted cells of the cyanobacterium Spirulina platensis. New Phytol. 141: 231-239.

    Google Scholar 

  • Masojídek J., Torzillo G., Koblízek M., Kopecký J., Bernardini P., Sacchi A. et al. 1999. Photoadaptation of two members of the Chlorophyta (Scenedesmus and Chlorella) in laboratory and outdoor cultures: changes of chlorophyll fluorescence quenching and the xanthophyll cycle. Planta 209: 126-135.

    Google Scholar 

  • Masojídek J., Torzillo G., Koblízek M., Kopecký J., Nidiaci L., Komenda J. et al. 2000. Changes in chlorophyll fluorescence quenching and pigment composition in the green alga Chlorococcum sp. grown under nitrogen deficiency and salinity stress. J. appl. Phycol. 12: 417-426.

    Google Scholar 

  • Mathis P. and Schenck C.C. 1982. The function of carotenoids in photosynthesis. In: Britton G. and Goodwin T.W. (eds), Carotenoid chemistry and biochemistry. Pergamon, Oxford, pp. 339-352.

  • Nedbal L. and Whitmarsh J. 1992. Photosystem II reaction centers inactive in plastoquinone pool reduction: a brief review. Photosynthetica 27: 57-61.

    Google Scholar 

  • Niyogi K., Björkman O. and Grossman A.R. 1997. The roles of specific xanthophylls in photoprotection. Proc. natl Acad. Sci USA 94: 14162-14167.

    Google Scholar 

  • Olaizola M. 2000. Commercial production of astaxanthin from Haematococcus pluvialis using 25,000-liter outdoor photobioreactors. J. appl. Phycol. 12: 499-506.

    Google Scholar 

  • Rippka R., Deruelles J.B., Herdman M., Waterbury B. and Stanier R.Y. 1979. Assignments, strain history and properties of pure cultures of Cyanobacteria. J. gen. Microbiol. 111: 1-61.

    Google Scholar 

  • Schreiber U. and Bilger W. 1987. Rapid assessment of stress effects on plant leaves by chlorophyll fluorescence measurements. In: Tenhunen G.D. (ed.), Plant Response to Stress. Springer-Verlag, New York, pp. 27-53.

    Google Scholar 

  • Schreiber U. and Neubauer C. 1987. The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: II. Partial control by the photosystem II donor side and possible ways of interpretation. Z. Naturforsh. 42: 1255-1264.

    Google Scholar 

  • Shoefs B., Rmiki N.E., Rachadi J. and Lemoine Y. 2001. Astaxanthin accumulation in Haematococcus requires a cytochrome P450 hydroxylase and an active synthesis of fatty acids. FEBS Lett. 500: 125-128.

    Google Scholar 

  • Srivastava A., Guissé B., Greppin H. and Strasser R. 1997. Regulation of antenna structure and electron transport in photosystem II of Pisum sativum under elevated temperature probed by the fast polyphasic chlorophyll a fluorescence transient: OKJIP. Biochim. biophys. Acta 1320: 95-106.

    Google Scholar 

  • Srivastava A.M., Strasser R.J. and Govindjee 1999. Greening of pea leaves: parallel measurements of 77K emission spectra,OJIP chlorophyll a fluorescence transient, period four oscillation of initial fluorescence level, delayed light emission, and P700. Photosynthetica 37: 365-392.

    Google Scholar 

  • Strasser R.J., Srivastava A. and Govindjee 1995. Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem. Photobiol. 61: 33-42.

    Google Scholar 

  • Trtílek M., Kramer D.M., Koblizek M. and Nedbal L. 1997. Dualmodulation LED kinetic fluorometer. J. Lumin. 72-74: 597- 599.

    Google Scholar 

  • van Kooten O. and Snel J.F.H. 1990. The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth. Res. 25: 147-145.

    Google Scholar 

  • Vass I., Kirilovsky D. and Etienne A.L. 1999. UV-B radiation-induced donor-and acceptor-side modifications of photosystem II in the cyanobacterium Synechococcus sp. PCC 6803. Biochemistry 38: 12786-12794.

    Google Scholar 

  • Vonshak A., Torzillo G., Masojidek J. and Boussiba S. 2001. Suboptimal morning temperature induces photoinhibition in dense outdoor cultures of the alga Monodus subterraneus (Eustigmatophyta) Plant Cell. Envir. 24: 1113-1118.

    Google Scholar 

  • Young Y.Y.R. and Lee Y.K. 1991. Do carotenoids play a photoprotective role in the cytoplasm of Haematococcus lacustris (Chlorophyta)? Phycologia 30: 257-261.

    Google Scholar 

  • Zlotnik I., Sukenik A. and Dubinsky Z. 1993. Physiological and photosynthetic changes during the formation of red aplanospore in the Chlorophyte Haematococcus pluvialis. J. Phycol. 29: 463-469.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Sezione di Firenze, Istituto per lo Studio degli Ecosistemi del CNR, Piazzale delle Cascine, Firenze, 28 I-50144, Italy

    G. Torzillo & C. Faraloni

  2. Faculty of Fisheries, Department of Aquaculture, Ege University, Bornova, 3100, Turkey

    T. Goksan

  3. Institute of Microbiology, Academy of Sciences, Trebon, CZ-37981, Czech Republic

    J. Kopecky & J. Masojídek

  4. Institute of Physical Biology, University of South Bohemia, Nove Hrady, CZ-37333, Czech Republic

    J. Kopecky & J. Masojídek

Authors
  1. G. Torzillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Goksan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Faraloni
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Kopecky
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Masojídek
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Torzillo, G., Goksan, T., Faraloni, C. et al. Interplay between photochemical activities and pigment composition in an outdoor culture of Haematococcus pluvialis during the shift from the green to red stage. Journal of Applied Phycology 15, 127–136 (2003). https://doi.org/10.1023/A:1023854904163

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1023854904163

Search

Navigation