Recent plastid replacement in Karlodinium ballantinum (Kareniaceae, Dinoflagellata) challenges the paradigms of endosymbiotic gene transfer

Plastids, the photosynthetic organelles of eukaryotes, arose via endosymbiosis of cyanobacteria by a eukaryotic host and were subsequently spread across eukaryotic diversity by additional endosymbioses. The process of plastid endosymbiosis is poorly understood, as most endosymbiotic events happened long ago. One group of microbial eukaryotes, the dinoflagellates, are characterized by their highly convoluted plastid evolution, particularly the family Kareniaceae, who have replaced their ancestral dinoflagellate plastid in most members with haptophyte plastids. To further explore the evolutionary history of kareniacean plastids, we obtained transcriptomic data from two representatives: Gertia stigmatica and Karlodinium ballantinum. We determined that Gt. stigmatica retained its ancestral plastid and that it is nested deep within the Kareniaceae. Furthermore, the transcriptome shows no evidence of haptophyte plastid ancestry, indicating a haptophyte plastid was likely never present. Conversely, K. ballantinum has abundant gene transfers originating from haptophytes, shared with other Kareniaceae. Surprisingly, K. ballantinum's plastid genome is nearly identical to that of extant haptophyte Gephyrocapsa huxleyi, but we were unable to identify gene transfers from this current plastid across the transcriptome. We therefore conclude that i) the phylogenomic position of Gt. stigmatica and its retention of the ancestral plastid supports at least two independent plastid replacements in Kareniaceae, and ii) K. ballantinum has replaced its plastid organelle twice, with the second replacement being as yet unaccompanied by endosymbiotic gene transfer. Phylogenomics of plastid genomes suggests that the unusually high plastid replacement rate in Kareniaceae might be caused by accelerated mutation of the plastid genome within the host.