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, 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, Experientia, 49(8), 1993, pp. 614-623
The bioluminescent dinoflagellate Gonyaulax polyedra contains various
indoleamines, in particular, melatonin and 5-methoxytryptamine, as wel
l as enzymes of their biosynthetic pathway. Melatonin exhibits a high-
amplitude circadian rhythm characterized by a dramatic increase shortl
y 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. pol
yedra shows a short-day response, which consists in the formation of a
sexual cysts. Light break experiments demonstrate the photoperiodic na
ture of this reaction. Cells become sensitive to short days only upon
exposure to a lowered temperature ( < 16-degrees-C). Melatonin mimics
the short-day effect, but only at decreased temperature. 5-Methoxytryp
tamine is even a better inducer of cyst formation, acting also at 20-d
egrees-C and in any lighting schedule, including LL. Cyst induction is
associated with stimulation of bioluminescence and cytoplasmic acidif
ication. A model on the intracellular pathway of photoperiodic informa
tion transduction assumes increased deacetylation of melatonin under c
yst-inducing conditions, binding of 5-methoxytryptamine to the membran
e of an acidic vacuole, proton transfer to the cytoplasm, and decrease
d 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 substitut
ed kynuramine (AFMK). Destruction of melatonin by light-induced supero
xide anions in the presence of cellular hemin may represent a property
which, during evolution, has made this molecule suitable as an indica
tor of darkness. On the other hand, AFMK, which is formed under illumi
nation, might have become a mediator of the information 'light'. Photo
periodism in Gonyaulax shows surprising parallels to that in mammals,
but allows the analysis of this phenomenon at an entirely cellular lev
el.