Dinoflagellates are successful marine protists found in the oceans worldwide. Some are responsible for toxic blooms while others live in symbiotic relationships, either as mutualistic symbionts in corals or as parasites infecting other protists and animals. Dinoflagellates harbor atypically large genomes (~3 to 250 Gb), with gene organization and gene expression patterns very different from closely-related apicomplexan parasites. We investigated the very compact genomes (~115 Mb) of two early-diverging and co-occurring Syndiniales dinoflagellate species, Amoebophrya spp. A25 and A120, parasites of phototrophic dinoflagellates, to shed light on the emergence of such atypical genomic features. The cumulative effect of a small number of transposable elements, along with short introns and intergenic regions, and the limited number of gene families, together contribute to the compactness of the Amoebophrya genomes, a feature potentially linked with parasitism. While the majority of Amoebophrya proteins (63.7% of A25 and 59.3% of A120) had no functional assignment, we found many orthologs shared with Dinophyceae. Our analyses revealed a strong tendency for gene co-orientation and high levels of synteny between the two genomes despite low interspecific protein sequence similarity, suggesting rapid protein evolution. Most strikingly, we identified a large portion of non-canonical and sometimes repeated introns displaying a broad variability of associated splicing motifs never observed among eukaryotes. Those introner elements appear to have the capacity to spread over their respective genomes in a manner similar to transposable elements. Finally, we confirmed the reduction of organelles observed in Amoebophrya spp. (i.e., loss of the plastid, potential loss of a mitochondrial genome and functions). These results expand the range of atypical genome features found in basal dinoflagellates and raise questions regarding speciation and the evolutionary the evolutionary mechanisms at play while parastitism was selected for in this particular unicellular lineage.
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