Endosymbiotic Gene Transfer in Tertiary Plastid-Containing Dinoflagellates

Abstract

Plastid establishment involves the transfer of endosymbiotic genes to the host nucleus, a process known as endosymbiotic gene transfer (EGT). Large amounts of EGT have been shown in several photosynthetic lineages but also in present-day plastid-lacking organisms, supporting the notion that endosymbiotic genes leave a substantial genetic footprint in the host nucleus. Yet the extent of this genetic relocation remains debated, largely because the long period that has passed since most plastids originated has erased many of the clues to how this process unfolded. Among the dinoflagellates, however, the ancestral peridinin-containing plastid has been replaced by tertiary plastids on several more recent occasions, giving us a less ancient window to examine plastid origins. In this study, we evaluated the endosymbiotic contribution to the host genome in two dinoflagellate lineages with tertiary plastids. We generated the first nuclear transcriptome data sets for the "dinotoms," which harbor diatom-derived plastids, and analyzed these data in combination with the available transcriptomes for kareniaceans, which harbor haptophyte-derived plastids. We found low level of detectable EGT in both dinoflagellate lineages, with only 9 genes and 90 genes of possible tertiary endosymbiotic origin in dinotoms and kareniaceans, respectively, suggesting that tertiary endosymbioses did not heavily impact the host dinoflagellate genomes.

Genomic perspectives on the birth and spread of plastids

“…A similar picture can be drawn from a recent study of EGT in two tertiary plastid-bearing dinoflagellate lineages, the kareniaceans, which have a haptophyte-derived plastid, and the so-called "dinotoms," dinoflagellates with diatom plastids (88). A merit of the transcriptome-based datasets used in this analysis is that the tertiary acquisitions are relatively recent and the donor lineages (haptophytes and diatoms) are well defined, in principle making it easier to detect EGT against the dinoflagellate nuclear genomic background.…”

Current Knowledge and Recent Advances in Marine Dinoflagellate Transcriptomic Research

“…The dinoflagellates are the only eukaryotic lineage that has been shown to have undergone several plastid replacement events, where native plastids are replaced with those acquired from other algal groups [84]. Transcriptomic studies have played a key part in the relationships between photosynthetic and heterotrophic lineages of dinoflagellates, how organelles such as plastids have been gained and lost and have been vital for documenting gene transfer events between symbiont and host [86][87][88]. Further analysis of K. mikimotoi transcriptomic data revealed proof of events of independent plastid-to-host gene transfer in individual fucoxanthin plastid lineages acquired through tertiary endosymbiosis [87].…”

Integration of plastids with their hosts: Lessons learned from dinoflagellates

“…EST studies of fucoxanthin dinoflagellates have identified many gene transfers from the plastid to its host (70)(71)(72)(73). For example, in a recent study of the fucoxanthin dinoflagellates K. veneficum and Karenia brevis, Burki et al identified 90 ESTs of predicted haptophyte origin, including 34 that were predicted to encode a plastid targeting sequence, out of a total of 493 ESTs of definable phylogenetic affinity (74). Thus, ∼7% of the fucoxanthin dinoflagellate nuclear genome may encode proteins of haptophyte plastid origin, a figure approaching that found in other plastid lineages derived through secondary or tertiary endosymbiosis (9).…”

“…In the same study, the authors screened EST libraries of the dinotom algae K. foliaceum and D. baltica. Only 14 ESTs out of a total of 237 of definable phylogenetic origin resolved with diatoms, and none was predicted to encode a plastid-targeting sequence (74). The most recent study of gene transfer in Lepidodinium identified six ESTs, of probable green algal origin, that were predicted to contain a plastid-targeting sequence, from a total dataset of 4,746 sequences of both definable and uncertain phylogenetic origin (75).…”