Plastid dynamics during survival of Dinophysis caudata without its ciliate prey

To survive, the marine dinoflagellate Dinophysis caudata Saville-Kent must feed on the plastidic ciliate Myrionecta rubra (=Mesodinium rubrum), itself a consumer of cryptophytes. Whether D. caudata has its own permanent chloroplasts or retains plastids from its ciliate prey, however, remains unresolved. Further, how long D. caudata plastids (or kleptoplastids) persist and remain photosynthetically active in the absence of prey remains unknown. We addressed those issues here, using the first established culture of D. caudata. Phylogenetic analyses of the plastid 16S rRNA and psbA gene sequences directly from the three organisms (D. caudata, M. rubra, and a cryptophyte) revealed that the sequences of both genes from the three organisms are almost identical to each other, supporting that the plastids of D. caudata are kleptoplastids. A 3-month starvation experiment revealed that D. caudata can remain photosynthetically active for similar to 2 months when not supplied with prey. D. caudata cells starved for more than 2 months continued to keep the plastid 16S rRNA gene but lost the photosynthesis-related genes (i.e., psaA and psbA genes). When the prey was available again, however, D. caudata cells starved for more than 2 months were able to reacquire plastids and slowly resumed photosynthetic activity. Taken all together, the results indicate that the nature of the relationship between D. caudata and its plastids is not that of permanent cellular acquisitions. D. caudata is an intriguing protist that would represent an interesting evolutionary adaptation with regard to photosynthesis as well as help us to better understand plastid evolution in eukaryotes.