Analysis of Gambierdiscus transcriptome data supports ancient origins of mixotrophic pathways in dinoflagellates

Toxic dinoflagellates pose serious threats to human health and to fisheries. The genus Gambierdiscus is significant in this respect because its members produce ciguatoxin that accumulates in predominantly tropical marine food webs and leads to ciguatera fish poisoning. Understanding the biology of toxic dinoflagellates is crucial to developing control strategies. To this end, we generated a de novo transcriptome library from G. caribaeus and studied its growth under different culture conditions to elucidate pathways of carbon (C) and nitrogen (N) utilization. We also gathered available dinoflagellate transcriptome data to trace the evolutionary history of C and N pathways in this phylum. We find that rather than being specific adaptations to the epiphytic lifestyle in G. caribaeus, the majority of dinoflagellates share a large array of genes that putatively confer mixotrophy and the ability to use N via the ornithine-urea cycle and nitric oxide synthase production. These results suggest that prior to plastid endosymbiosis, the dinoflagellate ancestor possessed complex pathways that linked metabolism, intercellular signaling, and stress responses to environmental cues that have been maintained by extant photosynthetic species. This metabolic flexibility likely explains the success of dinoflagellates in marine ecosystems and may presage difficulties in controlling the spread of toxic species.