Dinophysis acuminata

Kleptoplastidy as a model for understanding early events in plastid endosymbiosis

Gene transfer from endosymbiont to host is a specific form of horizontal gene transfer (HGT) and is a critical process in the evolution of organelles including plastids. HGT from photosynthetic prey, rather than endosymbionts, is perhaps equally important in the evolution of organelles, but the prevalence of HGT is only now being recognized with increased genome sequencing. I am testing the hypothesis that HGT from prey can occur early in plastid acquisition and facilitate plastid retention using the dinoflagellate Dinophysis, which temporarily retains plastids stolen from algal prey.
stacks_image_74BB471F-879B-45A4-BEF6-160FED060D0F
SECOND-HAND PLASTID ACQUISITION IN THE DINOFLAGELLATE DINOPHYSIS ACUMINATA
The ciliate Myrionecta rubra retains the cryptophyte nucleus (A) and complete cryptophyte plastid and mitochondria (B), whereas Dinophysis acuminata only retains the plastid genome and inner two membranes (C).
The dinoflagellate Dinophysis is an ideal model organism for the study of HGT and plastid evolution in eukaryotes. The genus is exceptional among dinoflagellates, possessing plastids derived from cryptophyte algae. Dinophysis can be maintained in pure culture for several months but is ultimately mixotrophic and needs to feed to acquire plastids (a process known as kleptoplastidy). Dinophysis does not feed directly on the plastid source (the cryptophyte Geminigera cryophila), but rather on a ciliate (Myrionecta rubra) that has consumed the cryptophytes and retained their plastids. Despite the apparent absence of cryptophyte nuclear genes required for plastid function, Dinophysis can retain cryptophyte plastids for months without feeding.

To determine if this dinoflagellate has nuclear-encoded genes for plastid function, I sequenced cDNA from Dinophysis acuminata, its ciliate prey M. rubra, and the cryptophyte source of the plastid Geminigera cryophila. I identified plastid-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 plastid, 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 dearth of plastid-related genes compared to other fully phototrophic algae suggests that D. acuminata does not have the nuclear repertoire necessary to maintain the plastid permanently.
stacks_image_43E48E34-27A9-461E-A146-650D82BEB443
CELLULAR COMPARTMENT GOslim TERMS IN DINOPHYSIS ACUMINATA COMPARED TO OTHER FULLY PHOTOSYNTHETIC SPECIES.
For each species, the amount of cellular compartment GOslim terms is expressed as a percentage of the total number of annotations. The number of unigenes annotated by Blast2GO is listed below each species.