Evolutionary transition towards permanent chloroplasts? - Division of kleptochloroplasts in starved cells of two species of Dinophysis (Dinophyceae)

Abstract

Species within the marine toxic dinoflagellate genus Dinophysis are phagotrophic organisms that exploit chloroplasts (kleptochloroplasts) from other protists to perform photosynthesis. Dinophysis spp. acquire the kleptochloroplasts from the ciliate Mesodinium rubrum, which in turn acquires the chloroplasts from a unique clade of cryptophytes. Dinophysis spp. digest the prey nuclei and all other cell organelles upon ingestion (except the kleptochloroplasts) and they are therefore believed to constantly acquire new chloroplasts as the populations grow. Previous studies have, however, indicated that Dinophysis can keep the kleptochloroplasts active during long term starvation and are able to produce photosynthetic pigments when exposed to prey starvation. This indicates a considerable control over the kleptochloroplasts and the ability of Dinophysis to replicate its kleptochloroplasts was therefore re-investigated in detail in this study. The kleptochloroplasts of Dinophysis acuta and Dinophysis acuminata were analyzed using confocal microscopy and 3D bioimaging software during long term starvation experiments. The cell concentrations were monitored to confirm cell divisions and samples were withdrawn each time a doubling had occurred. The results show direct evidence of kleptochloroplastidic division and that the decreases in total kleptochloroplast volume, number of kleptochloroplasts and number of kleptochloroplast centers were not caused by dilution due to cell divisions. This is the first report of division of kleptochloroplasts in any protist without the associated prey nuclei. This indicates that Dinophysis spp. may be in a transitional phase towards possessing permanent chloroplasts, which thereby potentially makes it a key organism to understand the evolution of phototrophic protists.

Comparative ecophysiology of Dinophysis acuminata and D. acuta (DINOPHYCEAE, DINOPHYSIALES): effect of light intensity and quality on growth, cellular toxin content, and photosynthesis

“…Overall, results in this study highlight the different photosynthetic behavior in Teleaulax and Mesodinium relative to Dinophysis species, despite the fact that the latter seem to maintain some control over their kleptoplasts (Hansen et al 2016, Rusterholz et al 2017. In that sense, the only genetic clue so far to explain this observation has been the discovery of five proteins with photosynthetic function encoded in the nuclear genome of D. acuminata (Wisecaver and Hackett 2010).…”

“…, Rusterholz et al. ). In that sense, the only genetic clue so far to explain this observation has been the discovery of five proteins with photosynthetic function encoded in the nuclear genome of D. acuminata (Wisecaver and Hackett ).…”

Niche separation between different functional types of mixoplankton: results from NPZ-style N-based model simulations

“…The ability for kleptochloroplast maintenance lowers the need for frequent ingestion and a recent study even reported division of kleptochloroplasts in Dinophysis spp. (Rusterholz et al 2017). Photoacclimation, as proven in Mesodinium (Moeller et al 2011), also decreases photo-oxidative stress on chloroplasts and makes them last longer.…”

Uptake of Inorganic and Organic Nitrogen Sources by Dinophysis acuminata and D. acuta

“…This view is supported by observations of a gradual decline of the photosynthetic performance in old kleptoplastids relative to that of the newly acquired in well-fed cells [55]. Recently, Rusterholz et al [56] rejected the "dilution" theory and suggested a certain capacity of Dinophysis for kleptoplastid division, arguing in favour of a greater control than previously thought. In any case, starved condition led to a decline in kleptoplastid numbers per cell.…”