New plastids, old proteins: repeated endosymbiotic acquisitions in kareniacean dinoflagellates

Dinoflagellates are a diverse group of ecologically significant micro-eukaryotes that can serve as a model system for plastid symbiogenesis due to their susceptibility to plastid loss and replacement via serial endosymbiosis. Kareniaceae harbor fucoxanthin-pigmented plastids instead of the ancestral peridinin-pigmented ones and support them with a diverse range of nucleus-encoded plastid-targeted proteins originating from the haptophyte endosymbiont, dinoflagellate host, and/or lateral gene transfers (LGT). Here, we present predicted plastid proteomes from seven distantly related kareniaceans in three genera (Karenia, Karlodinium, and Takayama) and analyze their evolutionary patterns using automated tree building and sorting. We project a relatively limited (~ 10%) haptophyte signal pointing towards a shared origin in the family Chrysochromulinaceae. Our data establish significant variations in the functional distributions of these signals, emphasizing the importance of micro-evolutionary processes in shaping the chimeric proteomes. Analysis of plastid genome sequences recontextualizes these results by a striking finding the extant kareniacean plastids are in fact not all of the same origin, as two of the studied species (Karlodinium armiger, Takayama helix) possess plastids from different haptophyte orders than the rest. (Figure presented.) Kareniacean plastids are distinct from those of other dinoflagellates and are the result of at least three separate endosymbiotic events. Their proteomes, however, exhibit similar overall evolutionary signals and tend to preferentially utilize pre-existing genes left behind by the previous plastid iterations. Kareniacean plastid-targeted proteomes project relatively limited but consistent haptophyte-like signals. The patterns of the evolutionary chimerism in these proteomes suggest a degree of post-endosymbiotic diversification between individual genera and even species. Takayama helix and Karlodinium armiger have undergone additional plastid replacements while retaining similar plastid-targeted proteomes.