Plastid translocon recycling in dinoflagellates demonstrates the portability of complex plastids between hosts

The plastids of photosynthetic organisms on land are predominantly “primary plastids,” derived from an ancient endosymbiosis of a cyanobacterium. Conversely, the plastids of marine photosynthetic organisms were mostly gained through subsequent endosymbioses of photosynthetic eukaryotes generating so-called “complex plastids.” The plastids of the major eukaryotic lineages—cryptophytes, haptophytes, ochrophytes, dinoflagellates, and apicomplexans—were posited to derive from a single secondary endosymbiosis of a red alga in the “chromalveloate” hypothesis. Subsequent phylogenetic resolution of eukaryotes has shown that separate events of plastid acquisition must have occurred to account for this distribution of plastids. However, the number of such events and the donor organisms for the new plastid endosymbioses are still not resolved. A perceived bottleneck of endosymbiotic plastid gain is the development of protein targeting from the hosts into the new plastids, and this supposition has often driven hypotheses toward minimizing the number of plastid-gain events to explain plastid distribution in eukaryotes. But how plastid-protein-targeting is established for new endosymbionts is often unclear, which makes it difficult to assess the likelihood of plastid transfers between lineages. Here, we show that Kareniaceae dinoflagellates, which possess complex plastids known to be derived from haptophytes, acquired all the necessary protein import machinery from these haptophytes. Furthermore, cryo-electron tomography revealed that no additional membranes were added to the Kareniaceae complex plastid during serial endosymbiosis, suggesting that the haptophyte-derived import processes were sufficient. Our analyses suggest that complex red plastids are preadapted for horizontal transmission, potentially explaining their widespread distribution in algal diversity. •Plastid-protein translocons can be inherited with plastid transfers between organisms•Dinoflagellate Karlodinium veneficum plastids have only four bounding membranes•Four bounding membranes are not indicative of secondary endosymbioses only•Serial plastid replacement utilizes existing protein import systems Lewis et al. use dinoflagellate algae that have replaced their photosynthetic plastid organelles to investigate the processes of organelle establishment. They show that additional membranes are not always gained in serial endosymbioses and that key features of plastid-protein-targeting and maintenance can