Divergent and diversified proteome content across a serially acquired plastid lineage

Dinoflagellates are a diverse group of ecologically significant micro-eukaryotes, prone to the loss and replacement of their plastids via serial endosymbiosis. One such replacement took place in the ancestors of the Kareniaceae, which harbor haptophyte-derived plastids containing the pigment fucoxanthin, instead of the ancestral peridinin dinoflagellate plastid. The metabolic functions of the fucoxanthin plastid are performed by a diverse range of nucleus-encoded and plastid-targeted proteins, which may originate from the haptophyte ancestor of the fucoxanthin plastid, the peridinin-containing ancestor of the dinoflagellate host, and/or from lateral gene transfers. However, the evolutionary composition of fucoxanthin plastid proteomes across the diversity of kareniacean dinoflagellates remains poorly understood. Here, we determine the total composition of the plastid proteomes of seven distantly-related kareniacean dinoflagellates, including newly-sequenced members of three genera (Karenia, Karlodinium, and Takayama). Using a custom plastid-targeting predictor, automatic single-gene tree building and phylogenetic sorting of plastid-targeted proteins, we project relatively limited (~10%) and functionally distinctive contributions of the haptophyte endosymbiont to the fucoxanthin plastid proteome, in comparison to plastid-targeted proteins of dinoflagellate host origin. Considering a concatenated multigene phylogeny of haptophyte-derived plastid proteins, we show that the haptophyte order Chrysochromulinales is the closest living relative of the fucoxanthin plastid donor. We additionally perform detailed analyses of the N-terminal targeting sequences of kareniacean plastid signal peptides, reporting a surprisingly high sequence conservation. Finally, considering planetary-scale distributions of key kareniacean genera and haptophyte orders from Tara Oceans, we suggest ecological and mechanistic factors accompanying the endosymbiotic acquisition of the fucoxanthin plastid.