An endogenous annual clock in the toxic marine dinoflagellate Gonyaulax tamarensis

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Abstract
Blooms of the toxic dinoflagellate Gonyaulax tamarensis (synonyms Protogonyaulax tamarensis and Alexandrium tamarense) cause outbreaks of paralytic shellfish poisoning (PSP) in coastal waters throughout the world. In the Gulf of Maine, episodes occur between April and November, a seasonality due in part to life-cycle alternations between motile, vegetative cells and resting cysts which overwinter in bottom sediments. Newly formed cysts have a mandatory 2-6 month dormancy period during which germination is not possible, but once mature, the resting state will continue if temperatures are unfavourable or oxygen is unavailable. We now report another factor controlling germination of cysts of G. tamarensis from deep coastal waters--an endogenous annual clock that can override an otherwise favourable environment for germination. Similar annual variability in germination has not been observed for cysts of this species from shallow estuaries. These results represent the first conclusive demonstration of an endogenous circannual rhythm in a marine plant. They are evolutionarily and ecologically significant because an endogenous annual clock can lead to the release of motile cells into deep and relatively invariant bottom waters at those times when temperature and light at the surface are suitable for growth. In shallow waters where seasonal variability is large and extends to bottom sediments, a strategy similar to that of the seeds of terrestrial plants would be more appropriate, namely a direct coupling between germination and the external environment.