Plant superiority, the case of the Lingulodinium dinoflagellate.

Abstract

From prey to host to obligate symbiont: an intimate association between a ciliate and a dinoflagellate. The dinoflagellate Lingulodinium polyedra (presently Lingulodinium2 polyedrum) is known to produce bioluminescence and also to form harmful algal blooms (red tides). It has been the subject of numerous studies concerning its ecophysiology, biochemistry and molecular biology. The ciliate Strombidium cf. oculatum, isolated from the seawater in which the dinoflagellate bloomed, was found to naturally develop a temporary association with Lingulodinium. Following ingestion of Lingulodinium, the ciliate developed a temporary association with Lingulodinium, in which the algae continued to photosynthesize and grow within the ciliate. Our aim was to examine the nature of this association using several approaches, including pigment analysis, pulse amplitude modulated (PAM) fluorometry; transmission electron microscopy (TEM) and confocal laser scanning microscopy (CLSM). In the present study, using these methods, we show that Lingulodinium is able to survive within Strombidium for several days and to maintain its photosynthetic activity, as well as its viability, in the cytoplasm of the ciliate. Moreover, we show that Lingulodinium can undergo several cycles of cell division inside Strombidium. This is the first report of such an intimate association between a bloom-forming dinoflagellate and a ciliate. Our findings suggest that Lingulodinium is not merely a prey item for Strombidium but that an obligate symbiotic relationship may develop between them. Further studies are needed to determine the ecological implications of this association. We discuss how these findings, together with previously published reports, suggest that this association may be a more general phenomenon than previously thought. We propose that the association may be a potential strategy for both prey and predator under certain environmental conditions. Finally, we discuss how the observed association may have implications for the global carbon cycle.