Comparative Genomics of Endosymbiotically-Derived Organelles in Cryptophyte Algae

Abstract

The cryptophytes are an enigmatic group of unicellular algae that acquired their plastids through the process of secondary endosymbiosis, which involved the uptake and retention of a red algal endosymbiont. There are several eukaryotic lineages that contain red algal-derived secondary plastids, but the cryptophytes and chlorarachniophytes are unique among them in that along with the plastid, they have retained the vestigial endosymbiont nucleus, called the nucleomorph. The ability to study cryptophyte nucleomorph genome biology and evolution provides a unique opportunity to investigate the processes of genome reduction, gene loss, and endosymbiotic gene transfer that followed the establishment of red secondary plastids. Here, I present the complete nucleomorph and plastid genome sequences of the photosynthetic marine cryptophyte Chroomonas mesostigmatica CCMP1168. My comparative analysis of cryptophyte nucleomorph genomes shows that there is a highly conserved core gene set, including an ultra-conserved set of plastid-related genes, but that there is also lineage-specific gene loss. The presence of pseudogenes and relict open reading frames in areas of gene order conservation indicate that nucleomorph genome reduction via gene loss is still occurring. My comparative analysis of cryptophyte plastid genomes reveals that the plastid genome architecture of photosynthetic species has been incredibly slowly evolving compared to other red secondary plastids. In addition, the identification of several group II introns in the C. mesostigmatica plastid genome, possibly acquired through lateral gene transfer from more than one source, suggests that cryptophyte plastid genomes may be more affected by exogenous genetic material than previously thought. Using phylogenetic analyses of expanded cryptophyte nucleomorph and plastid gene sets, I attempt to resolve the tree of cryptophytes and to identify the closest modern day red algal ancestor of the cryptophyte plastid and nucleomorph. Although the nucleomorph and plastid gene phylogenies are not congruent, I highlight meaningful inferences made by combining the comparative genomic and phylogenomic data. In terms of gene content and genome architecture, the cryptophyte plastid and nucleomorph genomes are the most similar to modern-day red algae of all known red algal secondary plastid-containing lineages. Study of these organellar genomes continues to shed light on the evolution of photosynethic eukaryotes.