Dinophysis through good and lean times: exploring the phenology of a toxic marine dinoflagellate with a kleptoplastidic lifestyle
Victor Pochic  1, 2@  , Mathilde Schapira  2  , Thomas Lacour  3  , Bede Davies  4  , Pierre Gernez  1  
1 : Institut Des Substances et Organismes de la Mer - UR 2160
Nantes université - UFR des Sciences et des Techniques
2 : Laboratoire Environnement Ressources Morbihan-Pays de la Loire, Unité Littoral
Institut français de Recherche pour l'Exploitation de la Mer
3 : Laboratoire Physiologie des microalgues toxiques et nuisibles, Unité PHYTOX
Institut français de Recherche pour l'Exploitation de la Mer
4 : Institut Des Substances et Organismes de la Mer - UR 2160
Nantes université - UFR des Sciences et des Techniques

The planktonic dinoflagellate Dinophysis is a major source of concern in various coastal ecosystems worldwide, where it regularly contaminates edible shellfish with diarrhetic toxins. Dinophysis is also a peculiar biological model, that relies on specific kleptoplastidy (i.e. acquisition of plastids from a specific prey) for photosynthetic growth.

Using data from decades-long observation networks, we studied the phenology of Dinophysis in a diverse array of coastal sites along the French coastline, from the English Channel to the Mediterranean Sea. Based on cell counts from systematic microscope observation, we used Generalized Additive Models (GAMs) to model seasonal dynamics of Dinophysis and, when data was available, of its prey Mesodinium rubrum (a photosynthetic, kleptoplastidic ciliate). These analyses revealed that Dinophysis and Mesodinium abundances and growth exhibit clear, region-specific seasonal patterns. We compared these patterns to those of temperature and stratification of the water column, two hydrological parameters that shape the pelagic ecosystem. Moreover, in the two distinct regions for which M. rubrum observation data was available, we observed that periods of Dinophysis growth were concomitant with periods of high prey abundance, corroborated by the detection of high-biomass M. rubrum blooms on satellite images. This finding points towards a significant trophic link between Dinophysis and M. rubrum in the wild, for which concrete evidence is rather scarce in published research conducted in natural environments.

Finally, we focused on periods of low-to-no growth, when Dinophysis is hardly ever observed in situ. Starvation experiments on laboratory cultures of Dinophysis, combined with measurements of environmental DNA at several depths in one coastal site, help us draw hypotheses on the survival strategies of Dinophysis during the unfavourable winter period. Faced with the absence of prey, Dinophysis rapidly reduces its vegetative growth and photosynthetic activity. In accordance with previously published laboratory experiments, we observed that Dinophysis can survive long periods of starvation (>30 days) and successfully resume growth upon the return of its prey. Overall, our work offers new knowledge about a toxic marine microorganism whose blooms strongly affect shellfish farming worldwide, as well as insights into the ecology of an intriguing planktonic protist.


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