Advertisement

Experientia

, Volume 49, Issue 8, pp 614–622 | Cite as

The presence and function of melatonin and structurally related indoleamines in a dinoflagellate, and a hypothesis on the evolutionary significance of these tryptophan metabolites in unicellulars

  • R. Hardeland
Multi-Author Reviews Melatonin and the Light-Dark Zeitgeber in Vertebrates, Invertebrates and Unicellular Organisms

Abstract

The bioluminescent dinoflagellateGonyaulax polyedra contains various indoleamines, in particular, melatonin and 5-methoxytryptamine, as well as enzymes of their biosynthetic pathway. Melatonin exhibits a high-amplitude circadian rhythm characterized by a dramatic increase shortly after the onset of darkness. The maximum of melatonin is followed by a peak of 5-methoxytryptamine. These 5-methoxylated indoleamines seem to be involved in the mediation of the information ‘darkness’.G. polyedra shows a short-day response, which consists in the formation of asexual cysts. Light break experiments demonstrate the photoperiodic nature of this reaction. Cells become sensitive to short days only upon exposure to a lowered temperature (<16°C). Melatonin mimics the short-day effect, but only at decreased temperature. 5-Methoxytryptamine is even a better inducer of cyst formation, acting also at 20°C and in any lighting schedule, including LL. Cyst induction is associated with stimulation of bioluminescence and cytoplasmic acidification. A model on the intracellular pathway of photoperiodic information transduction assumes increased deacetylation of melatonin under cyst-inducing conditions, binding of 5-methoxytryptamine to the membrane of an acidic vacuole, proton transfer to the cytoplasm, and decreased intracellular pH as the stimulus for encystment. Melatonin shows the property of a scavenger of superoxide anions. This reaction, which is efficiently catalyzed by hemin, leads to the formation of a substituted kynuramine (AFMK). Destruction of melatonin by light-induced superoxide anions in the presence of cellular hemin may represent a property which, during evolution, has made this molecule suitable as an indicator of darkness. On the other hand, AFMK, which is formed under illumination, might have become a mediator of the information ‘light’. Photoperiodism inGonyaulax shows surprising parallels to that in mammals, but allows the analysis of this phenomenon at an entirely cellular level.

Key words

Circadian rhythms Gonyaulax indoleamines kynuramines melatonin 5-methoxytryptamine photoperiodism radicals 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Anderson, D. M., and Keafer, B. A., An endogenous annual clock in the toxic marine dinoflagellateGonyaulax tamarensis. Nature (London)325 (1987) 616–617.Google Scholar
  2. 2.
    Arendt, J., Role of the pineal gland in seasonal reproduction function in mammals. Oxford Rev. reprod. Biol.8 (1986) 266–320.Google Scholar
  3. 3.
    Balzer, I., Földesi, G., Behrmann, G., and Hardeland, R., Circadian variations in the sensitivity ofGonyaulax to kynuramine. Congr. Eur. Chronobiol., p. 22. Univ de Franche-Conté, Besançon 1989.Google Scholar
  4. 4.
    Balzer, I., and Hardeland, R., Influence of temperature on biological rhythms. Int. J. Biomet.32 (1988) 231–241.Google Scholar
  5. 5.
    Balzer, I., and Hardeland, R., Action of kynuramine in a dinoflagellate: stimulation of bioluminescence inGonyaulax polyedra. Comp. Biochem. Physiol.94C (1989) 129–132.Google Scholar
  6. 6.
    Balzer, I., and Hardeland, R., Stimulation of bioluminescence by 5-methoxylated indoleamines in the dinoflagellate,Gonyaulax polyedra. Comp. Biochem. Physiol.98C (1991) 395–397.Google Scholar
  7. 7.
    Balzer, I., and Hardeland, R., Induction of cyst formation by short photoperiods and 5-methoxylated indoleamines in a dinoflagellate,Gonyaulax polyedra. Eur. J. Cell Biol.54, suppl.32 (1991) 57.Google Scholar
  8. 8.
    Balzer, I., and Hardeland, R., Circadian variations in the effects of epinephrine, kynuramine and potential MAO inhibitors on bioluminescence ofGonyaulax, in: Chronobiology & Chronomedicine, pp. 16–22. Eds J. Surowiak and M. H. Lewandowski. Peter Lang, Frankfurt, Bern, New York, Paris 1991.Google Scholar
  9. 9.
    Balzer, I., and Hardeland, R., Circadian rhythmicity in the stimulation of bioluminescence by biogenic amines and MAO inhibitors inGonyaulax polyedra. Int. J. Biomet.34 (1991) 231–234.Google Scholar
  10. 10.
    Balzer, I., and Hardeland, R., Photopériodisme chez un organisme unicellulaire,Gonyaulax polyedra. Bull. Gr. Et. Rythmes Biol.23 (1991) 53.Google Scholar
  11. 11.
    Balzer, I., and Hardeland, R., Mechanism of cyst formation inGonyaulax polyedra: involvement of photoperiodism, low temperature, indoleamines and proton release. J. interdiscipl. Cycle Res.22 (1991) 87–88.Google Scholar
  12. 12.
    Balzer, I., and Hardeland, R., Photoperiodic control of encystment and role of indoleamines inGonyaulax. 20th Int. Conf. Chronobiol., abstract no. 18.2. Tel Aviv 1991.Google Scholar
  13. 13.
    Balzer, I., and Hardeland, R., Photoperiodism and effects of indoleamines in a unicellular alga,Gonyaulax polyedra. Science253 (1991) 795–797.PubMedGoogle Scholar
  14. 14.
    Balzer, I., and Hardeland, R., Effects of indoleamines and short photoperiods on the encystment ofGonyaulax polyedra. Chronobiol. Int.9 (1992) 260–265.PubMedGoogle Scholar
  15. 15.
    Balzer, I., and Hardeland, R., Fotoperiodismo y melatonina a nivel celular, estudio basado en el dinoflageladoGonyaulax polyedra. III Reunión de Grupos de Cronobiología, p. 11. Murcia 1992.Google Scholar
  16. 16.
    Balzer, I., and Hardeland, R., Une résponse photopériodique chez le dinoflagelléGonyaulax polyedra: le rôle possible des indoleamines. Bull. Gr. Et. Rythmes Biol.25, no. 4 (1993) 23–27.Google Scholar
  17. 17.
    Balzer, I., and Hardeland, R., On the mechanism of cyst induction inGonyaulax polyedra: roles of photoperiodism, low temperature, 5-methoxylated indoleamines, and proton release, in: Chronobiology & Chronomedicine. Eds C. Gutenbrunner, G. Hildebrandt and R. Moog. Peter Lang, Frankfurt Berlin/ Bern/New York/Paris/Wien 1993, pp. 127–133.Google Scholar
  18. 18.
    Balzer, I., and Hardeland, R., Effects of short-days, melatonin and 5-methoxytryptamine in the marine algaGonyaulax polyedra (Gonyaulacaceae). Proc. 27th Eur. mar. Biol. Symp. Dublin 1993. In press.Google Scholar
  19. 19.
    Balzer, I., Pöggeler, B., and Hardeland, R., Indoleamines in the circadian organization ofGonyaulax: evidence for presence and effects on bioluminescence. J. Interdiscipl. Cycle Res.20 (1989) 169.Google Scholar
  20. 20.
    Balzer, I., Pöggeler, B., and Hardeland, R., 5-Methoxylated indoleamines in the dinoflagellateGonyaulax polyedra: presence, stimulation of bioluminescence, and circadian variations in responsiveness. Eur. J. Cell Biol.51 (suppl.30) (1990) 52.Google Scholar
  21. 21.
    Balzer, I., Pöggeler, B., and Hardeland, R., Effects of indoleamines in the circadian organization ofGonyaulax, in: Chronobiology & Chronomedicine, pp. 9–15. Eds J. Surowiak and M. H. Lewandowski. Peter Lang, Frankfurt/Bern/New York/Paris 1991.Google Scholar
  22. 22.
    Balzer, I., Pöggeler, B., and Hardeland, R., Free-running circadian rhythm of melatonin in a dinoflagellate,Gonyaulax polyedra, in: Melatonin and the Pineal Gland. From Basic Science to Clinical Application (Satellite Symp. IXth Int. Congr. Endocrinol.), abstract no. 113. Paris 1992.Google Scholar
  23. 23.
    Balzer, I., Pöggeler, B., and Hardeland, R., Circadian rhythms of indoleamines in a dinoflagellate,Gonyaulax polyedra: Persistence of metatonin rhythm in constant darkness and relationship to 5-methoxytryptamine, in: Melatonin and the Pineal Gland. From Basic Science to Clinical Application. pp. 183–186. Eds Y. Touitou, F. Arendt and P. Pévet, Elsevier, Amsterdam 1993.Google Scholar
  24. 24.
    Banerjee, S., Kerr, V., Winston, M., Kelleher, J. K., and Margulis, L., Melatonin: inhibition of microtubule-based oral morphogenesis inStentor coeruleus. J. Protozool.19 (1972) 108–113.PubMedGoogle Scholar
  25. 25.
    Banerjee, S., and Margulis, L., Mitotic arrest by melatonin. Expl. Cell Res.78 (1973) 314–318.Google Scholar
  26. 26.
    Benitez-King, G., Huerto-Delgadillo, L., and Antón-Tay, F., Melatonin effects on cytoskeletal organization of MDKC and neuroblastoma NIE-115 cells. J. Pineal Res.9 (1990) 209–220.PubMedGoogle Scholar
  27. 27.
    Beck, O., and Jonsson, G.,In vivo formation of 5-methoxytryptamine from melatonin in rat. J. Neurochem.36 (1981) 2013–2018.PubMedGoogle Scholar
  28. 28.
    Busa, W. B., Cellular dormancy and the scope of pHi-mediated metabolic regulation, in: Intracellular pH: Its Measurement, Regulation and Utilization in Cellular Functions, pp. 417–426. Eds R. Nuccitelli and D. W. Deamer. Alan Liss, New York 1982.Google Scholar
  29. 29.
    Cahill, G. M., and Besharse, J. C., Retinal melatonin is metabolized within the eye ofXenopus laevis. Proc. natl. Acad. Sci. USA86 (1989) 1098–1102.PubMedGoogle Scholar
  30. 30.
    Costas, E., and Varela, M., Evidence of an endogenous circannual rhythm in growth rates in dinoflagellates. Chronobiologia15 (1988) 223–226.PubMedGoogle Scholar
  31. 31.
    Costas, E., and Varela, M., A circannual rhythm in cyst formation and growth rates in the dinoflagellateScripsiella trochoidea Stein. Chronobiologia16 (1989) 265–270.PubMedGoogle Scholar
  32. 32.
    Csaba, G., Ontogeny and Phylogeny of Hormone Receptors. Karger, Basel 1981.Google Scholar
  33. 33.
    Dunlap, J. C., Taylor, W., and Hastings, J. W., The control and expression of bioluminescence in dinoflagellates, in: Bioluminescence: Current Perspectives, pp. 108–124. Ed. K. H. Nealson. Burgess, Minneapolis 1981.Google Scholar
  34. 34.
    Finocchiaro, L., Callebert, J., Launay, J. M., and Jallon, J. M., Melatonin biosynthesis inDrosophila: its nature and its effects. J. Neurochem.50 (1988) 382–387.PubMedGoogle Scholar
  35. 35.
    Fritz, L., Morse, D., and Hastings, J. W., The circadian bioluminescence ofGonyaulax is related to daily variations in the number of light-emitting organelles. J.Cell Sci.95 (1990) 321–328.PubMedGoogle Scholar
  36. 36.
    Galzin, A. M., Eon, M. T., Esnaud, H., Lee, C. R., Pévet, P., and Langer, S. Z., Day-night rhythm of 5-methoxytryptamine biosynthesis in the pineal gland of the golden hamster (Mesocricetus auratus). J. Endocr.118 (1988) 389–397.PubMedGoogle Scholar
  37. 37.
    Hardeland, R., and Balzer, I., Proton transfer in the signal tranduction of biogenic amines inducing cyst formation inGonyaulax polyedra (Dinoflagellata). 5th Int. Congr. Cell Biol., p. 213. Madrid 1992.Google Scholar
  38. 38.
    Hardeland, R., and Balzer, I., Chronobiological organization of the marine dinoflagellate,Gonyaulax polyedra (Gonyaulacaceae): Periodicity as a cyclic expression of phenotypical characteristics and responses to changes in temperature and photoperiod. Proc. 27th Eur. mar. Biol. Symp. Dublin 1993. In press.Google Scholar
  39. 39.
    Hardeland, R., and Balzer, I., Chronobiology of unicells: Multiplicity of frequencies, non-oscillatory states, photoperiodism and effects of biogenic amines, in: Trends in Comparative Biochemistry and Physiology. Research Trends, Trivandrum 1993. In press.Google Scholar
  40. 40.
    Hardeland, R., Balzer, I., and Breuer, S., Effects of kynuramine, epinephrine and potential MAO inhibitors within the circadian rhythm of bioluminescence inGonyaulax. J. interdiscipl. Cycle Res.20 (1989) 188–189.Google Scholar
  41. 41.
    Hardeland, R., Balzer, I., und Pöggeler, B., Melatonin-Rhythmik und Photoperiodismus bei dem DinoflagellatenGonyaulax polyedra. Verh. dt. zool. Ges.85, Teil1, (1992) 113.Google Scholar
  42. 42.
    Hardeland, R., Balzer, I., Pöggeler, B., Behrmann, G., and Fuhrberg, B., Evolutionary aspects of circadian rhythmicity and indoleamine-mediated photoperiodism. Eur. J. Cell Biol.57, (suppl.36) (1992) 29.Google Scholar
  43. 43.
    Hardeland, R., Fuhrberg, B., Behrmann, G., and Balzer, I., Sleep-latency reducing pineal hormone melatonin as a scavenger of free radicals: hemin-catalysed formation of N1-acetyl-N2-formyl-5-methoxykynuramine. Sleep Res.22 (1993) 621.Google Scholar
  44. 44.
    Hardeland, R., Harnau, G., Volknandt, W., Rode, I., and Balzer, I., On the transitions between rhythmic and arrhythmic states of theGonyaulax circadian oscillator. Proc. 11th Int. Soc. Biometeorol. Congr., West Lafayette 1987, pp. 281–285. Eds D. Driscoll and E. O. Box. SPB Acad. Publ. bv, Den Haag 1989.Google Scholar
  45. 45.
    Hardeland, R., Pöggeler, B., Balzer, I., and Behrmann, G., Common basis of photoperiodism in phylogenetically distant organisms and its possible origins. J. interdiscipl. Cycle Res.22 (1991) 122–123.Google Scholar
  46. 46.
    Hardeland, R., Pöggeler, B., Balzer, I., and Behrmann, G., A hypothesis on the evolutionary origins of photoperiodism based on circadian rhythmicity of melatonin in phylogenetically distant organisms, in: Chronobiology & Chronomedicine, pp. 113–120. Eds C. Gutenbrunner, G. Hildebrandt and R. Moog. Peter Lang, Frankfurt/Berlin/Bern/New York/Paris/Wien 1993.Google Scholar
  47. 47.
    Hayaishi, O., and Yoshida, R., Rhythms and physiological significance of indoleamine 2,3-dioxygenase, in: Biological Rhythms and their Central Mechanism, pp. 133–141. Eds M. Suda, O. Hayaishi and H. Nakagawa. Elsevier, North Holland/ Amsterdam/New York/Oxford 1979.Google Scholar
  48. 48.
    Kubis, H.-P., Balzer, I., and Hardeland, R., Effects of 1,2-dihydro-4-hydroxy-6-methoxy-N-methyl quinoline in relation to circadian rhythms of NAD+ kinase and NADP+ autoreduction inNeurospora crassa and bioluminescence inGonyaulax polyedra. Comp. Biochem. Physiol.102C (1992) 97–101.Google Scholar
  49. 49.
    Morita, M., and Best, J. B., Effects of photoperiods and melatonin on planarian asexual reproduction. J. exp. Zool.231 (1984) 273–282.Google Scholar
  50. 50.
    Morse, D. S., Fritz, J., and Hastings, J. W., What is the clock? Translational regulation of circadian bioluminescence. Trends biochem. Sci.15 (1990) 262–265.PubMedGoogle Scholar
  51. 51.
    Nuccitelli, R., and Heiple, J. M., Summary of the evidence and discussion concerning the involvement of pHi in the control of cellular functions, in: Intracellular pH: Its Measurement, Regulation and Utilization in Cellular Functions, pp. 567–586. Eds R. Nuccitelli and D. W. Deamer. Alan Liss, New York 1982.Google Scholar
  52. 52.
    Pévet, P., Is 5-methoxytryptamine a pineal hormone? Psychoneuroendocrinology8 (1983) 61–73.PubMedGoogle Scholar
  53. 53.
    Pévet, P., The integration of environmental information in mammals: possible role of 5-methoxytryptamine, in: Advances in Pineal Research, vol. 2, pp. 127–134. Eds R. J. Reiter and F. Fraschini. John Libbey, London 1987.Google Scholar
  54. 54.
    Pévet, P., Vivien-Roels, B., and Masson-Pévet, M., Low temperature in the golden hamster accelerates the gonadal atrophy induced by short photoperiod but does not affect the daily pattern of melatonin secretion. J. neural Transm.76 (1989) 119–128.PubMedGoogle Scholar
  55. 55.
    Pöggeler, B., Vergleichende Untersuchungen über Melatonin und strukturverwandte Tryptophanmetabolite. Zur Rolle von Melatonin und 5-Methoxytryptamin bei einem Dinoflagellaten,Gonyaulax polyedra, sowie pinealen und extrapinealen 5-methoxylierten Indolaminen bei Vertebraten. Doctoral thesis, Göttingen 1992.Google Scholar
  56. 56.
    Pöggeler, B., Balzer, I., Fischer, J., Behrmann, G., and Hardeland, R., A role of melatonin in dinoflagellates? Acta endocr. (Copenh.)120 (suppl.1) (1989) 97.Google Scholar
  57. 57.
    Pöggeler, B., Balzer, I., Hardeland, R., and Lerchl, A., Pineal hormone melatonin oscillates also in the dinoflagellateGonyaulax polyedra. Naturwissenschaften78 (1991) 268–269.Google Scholar
  58. 58.
    Quentin, E., Wilde, J., Schilling, A. C., and Hardeland, R., Chronobiological experiments inGonyaulax polyedra andEuglena gracilis with heat-stable cytosolic extracts modulating protein synthesis, in: Chronobiology & Chronomedicine, pp. 55–59. Eds G. Hildebrandt, R. Moog and F. Raschke. Peter Lang, Frankfurt/Bern/New York/Paris 1987.Google Scholar
  59. 59.
    Raynaud, F., Miguel, J. L., Vivien-Roels, B., Masson-Pévet, M., and Pévet, P., The effect of 5-methoxytryptamine on golden hamster gonads is not a consequence of its acetylation into melatonin. J. Endocr.121 (1989) 507–512.PubMedGoogle Scholar
  60. 60.
    Raynaud, F., Vivien-Roels, B., Masson-Pévet, M., and Pévet, P., Plasma concentrations of 5-methoxytryptamine, 5-methoxytryptophol and melatonin after 5-methoxytryptamine administration of golden hamsters: physiological implications. J. neural Transm.84 (1991) 33–43.Google Scholar
  61. 61.
    Reiter, R. J., The pineal and its hormones in the control of reproduction in mammals. Endocr. Rev.1 (1980) 109–131.PubMedGoogle Scholar
  62. 62.
    Reiter, R. J., Action spectra, dose-response relationships, and temporal aspects of light's effects on the pineal gland. Ann. N. Y. Acad. Sci.453 (1985) 215–230.PubMedGoogle Scholar
  63. 63.
    Tamarkin, L., Baird, C. J., and Almeida, O. F. X., Melatonin. A coordinative signal for mammalian reproduction? Science227 (1985) 714–720.PubMedGoogle Scholar
  64. 64.
    Uemura, T., and Kadota, K., Serotonin- and melatonindependent light emission induced by xanthine oxidase, in: Progress in Tryptophan and Serotonin Research, pp. 673–676. Eds H. G. Schlossburger, W. Kochen, B. Linzen and H. Steinhart. Walter de Gruyter, Berlin 1984.Google Scholar
  65. 65.
    Uemura, T., Kanashiro, M., Yamano, T., Hirai, K., and Miyazaki, T., Isolation, structure, and properties of the β-carboline formed from 5-hydroxytryptamine by the superoxide anion-generating system. J. Neurochem.51 (1988) 710–717.PubMedGoogle Scholar
  66. 66.
    Vivien-Roels, B., Pévet, P., Beck, O., and Fèvre-Montagne, M., Identification of melatonin in the compound eye of an insect, the locust (Locusta migratoria) by radioimmunoassay and gas chromatography-mass spectrometry. Neurosci. Lett.49 (1984) 153–157.PubMedGoogle Scholar
  67. 67.
    Wetterberg, L., Hayes, D. K., and Halberg, F., Circadian rhythms of melatonin in the brain of the face fly,Musca autumnalis De Geer. Chronobiologia14 (1987) 377–381.PubMedGoogle Scholar
  68. 68.
    Yentsch, C. M., and Mangue, F. C., Evidence of an apparent annual rhythm in the toxic red tide dinoflagellateGonyaulax excavata. Int. J. Chronobiol.7 (1980) 77–84.Google Scholar
  69. 69.
    Yoshizawa, Y., Wakabayashi, K., and Shinozawa, T., Inhibition of planarian regeneration by melatonin. Hydrobiologia227 (1991) 31–40.Google Scholar

Copyright information

© Birkhäuser Verlag Basel 1993

Authors and Affiliations

  • R. Hardeland
    • 1
  1. 1.I. Zoologisches InstitutUniversität GöttingenGöttingen(Germany)

Personalised recommendations