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 prey, rather than endosymbionts, is perhaps equally important in the evolution of organelles, but with increased genome sequencing the prevalence of HGT is only now being recognized. This proposal tests 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. Thus far, five genes necessary for plastid function have been identified in Dinophysis, and phylogenetic analyses indicate that the majority of these genes were acquired through HGT. A comprehensive survey of genes in Dinophysis is required to identify the full complement of plastid-targeted genes and determine their phylogenetic origin. A strong correlation between HGT and genes targeted to the stolen plastid would provide strong support for the hypothesis. These results will elucidate the relationship between HGT and plastid acquisition in Dinophysis.
The data collected with this research will be used to evaluate a different strategy of organelle acquisition than that outlined in the traditional endosymbiotic theory, one that begins with a predator-prey relationship rather than a mutualistic host-endosymbiont relationship. This study will include the training of an undergraduate student. In addition, this dataset will be available to the broader scientific community to investigate other aspects of Dinophysis, which have a major impact on global fisheries and human health through their production of toxins causing diarrhetic shellfish poisoning.
Intellectual Merit 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. We 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. Broader Impacts This project contibuted to the education and professional development of a Ph.D. student and and undergradaute student.
