On the primary functions of melatonin in evolution: Mediation of photoperiodic signals in a unicell, photooxidation, and scavenging of free radicals *

Abstract: Melatonin is widely abundant in many eukaryotic taxa, including vari‐ous animal phyla, angiosperms, and unicells. In the bioluminescent dinoflagellate Gonyaulax polyedra, melatonin is produced in concentrations sometimes exceed‐ing those found in the pineal gland, exhibits a circadian rhythm with a pro‐nounced nocturnal maximum, and mimics the short‐day response of asexual encystment. Even more efficient as a cyst inducer is 5‐methoxytryptamine (5MT), which is also periodically formed in Gonyaulax. In this unicell, the photoperiodic signal‐transduction pathway presumably involves melatonin formation, its deace‐tylation to 5MT, 5MT‐dependent transfer of protons from an acidic vacuole, and cytoplasmic acidification. According to this concept, we observe that cyst forma‐tion can be induced by various monoamine oxidase inhibitors and protonophores, that 5MT dramatically stimulates H+‐dependent bioluminescence and leads to a decrease of cytoplasmic pH, as shown by measurements of dicyanohydroquinone fluorescence. Cellular components from Gonyaulax catalyze the photooxidation of melatonin. Its property of being easily destroyed by light in the presence of cel‐lular catalysts may have been the reason that many organisms have developed mechanisms utilizing this indoleamine as a mediator of darkness. Photooxidative reactions of melatonin, as studied with crude Gonyaulax extracts and, more in de‐tail, with protoporphyrin IX as a catalyst, lead to the formation of N1 ‐acetyl‐N ‐formyl‐5‐methoxykynuramine (AFMK) as one of the main products. Photochemical mechanisms involve interactions with a photooxidant cation radi‐cal leading to the formation of a melatonyl cation radical, which subsequently combines with a superoxide anion. Photooxidation of melatonin represents one of several possibilities of a more general, biologically highly important property of this indoleamine to act as an extremely efficient radical scavenger, including its feature of terminating radical reaction chains by a final combination with the su‐peroxide anion. Trapping of free radicals may reflect the primary and evolutionar‐ily most ancient role of melatonin in living beings.