Horizontal gene transfer maintains chloroplasts stolen from prey in the algae Dinophysis acuminata

Dinophysis is an exceptional species of algae that possesses temporary chloroplasts acquired by feeding on photosynthetic prey. Although Dinophysis can be maintained in pure culture for several months, the genus is mixotrophic and needs to feed to reacquire chloroplasts. The extended length of time between feedings is surprising considering that Dinophysis presumably lacks thousands of prey nuclear genes required for chloroplast function. One possible mechanism for the longevity of these stolen chloroplasts is that Dinophysis has acquired its own suite of chloroplast-related genes through horizontal gene transfer, which would make Dinophysis an excellent model for studying the early events in chloroplast endosymbiosis. I sequenced cDNA from Dinophysis acuminata and the algal source of the chloroplast, Geminigera cryophila, and identified chloroplast-targeted proteins encoded in the nuclear genome of D. acuminata that function in photosystem stabilization, carbon fixation, and metabolite transport. Phylogenetic analyses show that the genes are derived from multiple algal sources indicating a complex evolutionary history involving horizontal gene transfer. These findings suggest that D. acuminata has some functional control of its stolen chloroplast, and may be able to extend the useful life of the stolen organelle by replacing damaged transporters and protecting components of the photosystem from stress. However, the overall dearth of chloroplast-related genes compared to other fully phototrophic algae suggests that D. acuminata does not have the nuclear repertoire necessary to maintain the chloroplast permanently. These findings suggest that horizontal gene transfer occurs early in, and may even facilitate the development of, chloroplast endosymbioses.