Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features

Abstract

The green lineage is reportedly 1,500 million years old, evolving shortly after the endosymbiosis event that gave rise to early photosynthetic eukaryotes. In this study, we unveil the complete genome sequence of an ancient member of this lineage, the unicellular green alga Ostreococcus tauri (Prasinophyceae). This cosmopolitan marine primary producer is the world's smallest free-living eukaryote known to date. Features likely reflecting optimization of environmentally relevant pathways, including resource acquisition, unusual photosynthesis apparatus, and genes potentially involved in C(4) photosynthesis, were observed, as was downsizing of many gene families. Overall, the 12.56-Mb nuclear genome has an extremely high gene density, in part because of extensive reduction of intergenic regions and other forms of compaction such as gene fusion. However, the genome is structurally complex. It exhibits previously unobserved levels of heterogeneity for a eukaryote. Two chromosomes differ structurally from the other eighteen. Both have a significantly biased G+C content, and, remarkably, they contain the majority of transposable elements. Many chromosome 2 genes also have unique codon usage and splicing, but phylogenetic analysis and composition do not support alien gene origin. In contrast, most chromosome 19 genes show no similarity to green lineage genes and a large number of them are specialized in cell surface processes. Taken together, the complete genome sequence, unusual features, and downsized gene families, make O. tauri an ideal model system for research on eukaryotic genome evolution, including chromosome specialization and green lineage ancestry.

Fig. 1.

General characteristics of the 20 O. tauri chromosomes. TEs, transposon frequency. Size is indicated to the left of each chromosome (Mb). Colored bars indicate the percentage G+C content (upper bar) and of transposons (lower bar).

Fig. 2.

Genome size and gene density for various eukaryote genomes. Cp, Cryptosporidium parvum; Ag, Ashbya gossypii, Sp, Schizosaccharomyces pombe; Sc, Saccharomyces cerevisiae; Ot, Ostreococcus tauri; Cm, Cyanydioschyzon merolae; Eh, Entamoeba hemolytica; Af, Aspergillus fumigatu; An, Aspergillus niger; Dd, Dictyostelium discoidum; Tp, Thalassiosira pseudonana; Ao, Aspergillus oryzae; Nc, Neurospora crassa; Ce, Caenorhabditis elegans; At, Arabidopsis thaliana; Dm, Drosophila melanogaster; Hs, Homo sapiens.

Fig. 3.

Taxon distribution of best hits for genes from each of the O. tauri chromosomes. Green, viridiplantae; blue, no hit; yellow, bacteria; red, metazoa; pink, fungi; gray, mycetozoa; orange, alveolates; purple, others. Annotation of genes on the low G+C part of chromosome 2 is difficult, and the percentage of genes having no hit on chromosome 2 can be slightly overestimated. See Genome Heterogeneity for details.