, Volume 193, Issue 1, pp 38–43 | Cite as

Carotenoids in the eyespot apparatus of the flagellate green alga Spermatozopsis similis: Adaptation to the retinal-based photoreceptor

  • Merete Grung
  • Georg Kreimer
  • Michael Calenberg
  • Michael Melkonian
  • Synnøve Liaaen-Jensen


Isolated intact eyespot apparatuses, the photoreceptive organelles involved in blue-light-mediated photoresponses of flagellate green algae, were analyzed regarding their carotenoid composition. Carotenoids from the eyespot apparatuses of Spermatozopsis similis were identified by high-performance liquid chromatography, visible-light absorption spectra, mass spectroscopy and by 1H-nuclear magnetic resonance spectroscopy (carotenes), and compared with those of whole-cell extracts. Both extracts contained β,β-carotene, β,ψ-carotene (formerly γ-carotene), lycopene, lutein, zeaxanthin, violaxanthin and all-E-and 9′-Z-neoxanthin. The relative carotenoid compositions, however, differed significantly. A twofold relative increase in the total carotene level was evident in the fraction enriched in eyespot apparatuses. This was mainly due to an increase in the monocyclic β,ψ-carotene and the aliphatic lycopene, whereas the relative content of β,β-carotene remained unchanged. On the other hand a relative decrease in the total xanthophyll content, especially of lutein and the epoxidic carotenoid neoxanthin, was observed in the eyespot apparatuses compared with the whole-cell extracts. The decrease of the latter resulted almost solely from a reduction of the 9′-Z-rather than the all-E-isomer. The bulk of the carotenes is thought to be localized in the highly organized eyespot lipid globules, which act as a combined quarter-wave interference reflector and absorption screen for the photoreceptor in green algae. The enrichment of β,ψ-carotene and lycopene in the eyespot apparatuses, extending the range of visible light absorption to longer wavelengths, represents an adaptation of the screen to the retinal-based photoreceptor of flagellate green algae and is one of the prerequisites for maximal directional sensitivity of the eyespot apparatus.

Key words

Carotenoid Eyespot apparatus Green algae Phototaxis Photoreceptor screen Spermatozopsis 



nuclear magnetic resonance


International Union of Pure and Applied Chemistry


visible absorption spectra


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  1. Batra, P.P., Tollin, G. (1964) Phototaxis in Euglena. I. Isolation of the eyespot granules and identification of the eyespot pigments. Biochim. Biophys. Acta 79, 371–378Google Scholar
  2. Beckmann, M., Hegemann, P. (1991) In vitro identification of rhodopsin in the green alga Chlamydomonas. Biochemistry 30, 3692–3697Google Scholar
  3. Ben-Amotz, A., Katz, A., Avron, M. (1982) Accumulation of β- carotene in halotolerant algae: purification and characterization of β-carotene rich globules from Dunaliella bardawil. J. Phycol. 18, 529–537Google Scholar
  4. Boscov, J.S., Feinleib, M.E. (1979) Phototactic response of Chlamydomonas to flashes of light. II. Response of individual cells. Photochem. Photobiol. 30, 499–505Google Scholar
  5. Davies, B.H. (1965) Analysis of carotenoid pigments. In: Chemistry and biochemistry of plant pigments, pp. 498–532, Goodwin, T.W., ed. Academic Press, LondonGoogle Scholar
  6. Derguini, F., Mazur, P., Nakanishi, K., Starace, D.M., Saranak, J., Foster, K.W. (1991) All-trans-retinal is the chromophore bound to the photoreceptor of the alga Chlamydomonas reinhardtii. Photochem. Photobiol. 54, 1017–1021Google Scholar
  7. Foster, K.W., Smyth, R.D. (1980) Light antennas in phototactic algae. Microbiol. Rev. 44, 572–630Google Scholar
  8. Foster, K.W., Saranak, J., Patel, N., Zarilli, G., Okabe, M., Kline, T., Nakanishi, K. (1984) A rhodopsin is the functional photoreceptor for phototaxis in the unicellular eukaryote Chlamydomonas. Nature 311, 756–759Google Scholar
  9. Goodwin, T.W. (1976) Distribution of carotenoids. In: Chemistry and biochemistry of plant pigments, vol. 1, pp. 225–261, Goodwin, T.W., ed. Academic Press, LondonGoogle Scholar
  10. Goodwin, T.W., ed. (1980) The biochemistry of the carotenoids, Vol. 1, Plants, 2nd edn., Chapman and Hall, LondonGoogle Scholar
  11. Grung, M., Metzger, P., Berkaloff, C., Liaaen-Jensen, S. (1993) Studies on the formation and localization of primary and secondary carotenoids in Botryococcus braunii, including the regreening process. Comp. Biochem. Physiol., in pressGoogle Scholar
  12. Harz, H., Hegemann, P. (1991) Rhodopsin-regulated calcium currents in Chlamydomonas. Nature 351, 489–491Google Scholar
  13. Harz, H., Nonnengässer, C., Hegemann, P. (1992) The photoreceptor current of the green alga Chlamydomonas. Philos. Trans. R. Soc. London B 338, 39–52Google Scholar
  14. Heelis, D.V., Kernick, W., Phillips, G.O., Davies, K. (1979) Separation and identification of the carotenoid pigments of stigmata isolated from light-grown cells of Euglena gracilis strain. Z. Arch. Microbiol. 121, 207–211Google Scholar
  15. Hegemann, P., Harz, H. (1993) Photoreception in Chlamydomonas. A multidisciplinary challenge. In: Signal transduction: Prokaryotic and simple eukaryotic systems, pp. 279–307, Kurjan, J., Taylor, B.L., eds. Academic Press, San DiegoGoogle Scholar
  16. Hegemann, P., Gärtner, W., Ihl, R. (1991) All-trans-retinal constitutes the functional chromophore in Chlamvdomonas rhodopsin. Biophys. J. 60, 1477–1489Google Scholar
  17. International Union of Pure and Applied Chemistry (IUPAC) (1974) Nomenclature of carotenoids. Rules approved 1974. Butterworths, LondonGoogle Scholar
  18. Ke, B., Imsgard, F., Kjøsen, H., Liaaen-Jensen, S. (1970) Electronic spectra of carotenoids at 77° K. Biochim. Biophys. Acta 210, 139–152Google Scholar
  19. Kreimer, G. (1993) Cell biology of phototaxis in flagellate algae. Int. Rev. Cytol. 148, 229–310Google Scholar
  20. Kreimer, G., Melkonian, M. (1990) Reflection confocal laser scanning microscopy of eyespots in flagellated green algae. Eur. J. Cell Biol. 53, 101–111Google Scholar
  21. Kreimer, G., Brohsonn, U., Melkonian, M. (1991 a) Isolation and partial characterization of the photoreceptive organelle for phototaxis of a flagellate green alga. Eur. J. Cell Biol. 55, 318–327Google Scholar
  22. Kreimer, G., Marner, F.-J., Brohsonn, U., Melkonian, M. (1991b) Identification of 11-cis and all-trans-retinal in the photoreceptive organelle of a flagellate green alga. FEBS Lett. 293, 49–52Google Scholar
  23. Kreimer, G., Overländer, C., Sineshchekov, O.A., Stolzis, H., Nultsch, W., Melkonian, M. (1992) Functional analysis of the eyespot in Chlamydomonas reinhardtii mutant ey 627, mt-. Planta 188, 513–521Google Scholar
  24. Lawson, M.A., Zacks, D.N., Derguini, F., Nakanishi, K., Spudich, J.L. (1991) Retinal analog restoration of phobic responses in a blind Chlamydomonas reinhardtii mutant. Biophys. J. 60, 1490–1498Google Scholar
  25. Melkonian, M., Robenek, H. (1984) The eyespot apparatus of flagellated green algae: a critical review. Prog. Phycol. Res. 3, 193–268Google Scholar
  26. Nultsch, W., Häder, D.-P. (1988) Photomovement in motile microorganisms — II. Photochem. Photobiol. 47, 837–869Google Scholar
  27. Ohad, I., Goldberg, I., Broza, R., Schuldiner, S., Gan-Zvi, E. (1969) Changes in lipid and pigment composition and photosynthetic activity during formation of chloroplast lamellae in a mutant of Chlamydomonas reinhardi y-1. In: Progress in photosynthesis research, vol. 1, pp. 284–295, Metzner, H., ed. International Union of Biological Sciences, TübingenGoogle Scholar
  28. Preisig, H.R., Melkonian, M. (1984) A light and electron microscopical study of the green flagellate Spermatozopsis similis spec. nova. Plant Syst. Evol. 146, 57–74Google Scholar
  29. Rüffer, U., Nultsch, W. (1991) Flagellar photoresponses of Chlamydomonas cells held on micropipettes: II. Change in flagellar beat pattern. Cell Motil. 18, 269–278Google Scholar
  30. Schiedt, K., Liaaen-Jensen, S. (1994) Isolation and analysis. In: Carotenoids, vol. 1A, Britton, G., Liaaen-Jensen, S., Pfander, H., eds. Birkhäuser, Basel, in pressGoogle Scholar
  31. Schlösser, U.G. (1986) Sammlung von Algenkulturen Göttingen: additions to the collection since 1984. Ber. Deutsch. Bot. Ges. 99, 161–168Google Scholar
  32. Sineshchekov, O.A. (1991) Electrophysiology of photomovements in flagellated algae. In: Biophysics of photoreceptors and photomovements, pp. 191–202, Lenci, F., ed. Plenum Press, New YorkGoogle Scholar
  33. Straub, O. (1987) Key to carotenoids. Pfander, H., Gerspacher, M., Rychener, M., Schwabe, R., eds. Birkhäuser, BaselGoogle Scholar
  34. Vetter, W., Englert, G., Rigassi, N., Schwieter, U. (1971) Spectroscopic methods. In: Carotenoids. pp. 189–266, Isler, O., ed. Birkhäuser, BaselGoogle Scholar
  35. Withers, N., Haxo, F.T. (1975) Chlorophyll c1 and c2 and extraplastidic carotenoids in the dinoflagellate, Peridinium foliaceum Stein. Plant Sci. Lett. 5, 7–15Google Scholar
  36. Withers, N.W., Haxo, F.T. (1978) Isolation and characterization of carotenoid-rich lipid globules from Peridinium foliaceum. Plant Physiol. 62, 36–39Google Scholar
  37. Zacks, D.N., Derguini, F., Nakanishi, K., Spudich, J. (1993) Comparative study of phototactic and photophobic receptor chromophore properties in Chlamydomonas reinhardtii. Biophys. J. 65, 508–518Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • Merete Grung
    • 1
  • Georg Kreimer
    • 2
  • Michael Calenberg
    • 2
  • Michael Melkonian
    • 2
  • Synnøve Liaaen-Jensen
    • 1
  1. 1.University of Trondheim, Norwegian Institute of Technology, Organic Chemistry LaboratoriesTrondheim-NTHNorway
  2. 2.Universität zu Köln, Botanisches InstitutKölnGermany

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