Horizontal Gene Transfer and Plastid Endosymbiosis in Dinoflagellate Gene Innovation

Abstract

Recent studies suggest that horizontal gene transfer (HGT) plays an important role in niche adaptation in some eukaryotes and may be a major evolutionary force in unicellular lineages. One subcategory of HGT is endosymbiotic gene transfer (EGT), which is characterized by a large influx of genes from endosymbiont to host nuclear genome and is a critical step in the establishment of permanent organelles, such as plastids. The dinoflagellates are a diverse group of mostly marine eukaryotes that have a propensity for both HGT and plastid endosymbiosis. Many dinoflagellates are predators and can acquire both genes and plastids from prey, blurring the distinction between HGT and EGT. Here, I measure genome mosaicism in dinoflagellates to investigate how HGT has impacted gene innovation and plastid endosymbiosis in this group. Because analysis of HGT depends on accurate phylogenetic trees, I first assessed the sensitivity of automated phylogenomic methods to variation in taxon sampling due to homolog selection parameters. Using methods based on this analysis, I showed that a large amount of HGT has occurred in dinoflagellates, particularly from bacterial donors. Further, I demonstrated that the dinoflagellate Alexandrium tamarense has the largest number of genes gained relative to related eukaryotes using ancestral gene content reconstruction. Additionally, dinoflagellates have lost several ubiquitous eukaryotic metabolic genes, but missing genes have been functionally replaced by xenologs from many evolutionarysources. Other transferred genes are involved in diverse functions. These results suggest that dinoflagellate genomes are heavily impacted by HGT. Also, I investigated the timing and consequences of HGT in plastid endosymbiosis. Using the dinflagellate Dinophysis acuminata, a mixotrophic species that sequesters and maintains prey plastids, I identified plastid-targeted proteins that function in photosystem stabilization and metabolite transport. Dinophysis acuminate may be able to extend the useful life of the stolen plastid by protecting the photosystem and replacing damaged transporters. Phylogenetic analyses showed that genes are derived from multiple sources indicating a complex evolutionary history involving HGT. Dinophysis acuminate can acquire both genes and plastids from prey, which suggests that HGT could play an important role in plastid acquisition during the earliest stages of this transition.