Comparative genomic studies on Dicyema japonicum: the phylogenetic position of dicyemids and the genomic adaptations to parasitic lifestyle

Parasitism has independently occurred more than 200 times across 15 animal phyla, yet remains a topic of debate how free-living ancestors evolved to parasitic organisms. Dicyemid mesozoans are microscopic endoparasites inhabiting the renal sacs of some cephalopods. They possess simplified body architecture without differentiated organs and have long fascinated biologists because of their incompletely known lifecycles. Obtaining genomic data from enigmatic parasites would be essential to better comprehend parasitism evolution. Here I decoded the genome of Dicyema japonicum which is approximately 68 Mbp with extraordinarily shortened introns. Comparing among bilaterians, D. japonicum retains fewer genes in most KEGG pathways, as in the case of four parasite species from different phyla that shows a convergent gene number reduction in the metabolism pathways. In contrast, D. japonicum exhibits multi-copy gene clusters associated with endocytosis and membrane trafficking, perhaps reflecting its specialized nutrient-uptake strategy. Up-regulated transcripts at dispersal larvae stage present over-representation on gene ontology terms of motor activity and response to the stimulus. The occurrences of neurotransmitters and neuropeptides on apical cells of dispersal larva was evident. Taken together, dicyemids may utilize potential sensory functions to detect the environmental cues and could actively approach new hosts. In summary, the dicyemid genome provides a resource to uncover mysterious lifecycle of dicyemids, as well as studying comparative genomics to gain insights into the parasitism evolution. Furthermore, genomes of parasites may adapt through eliminating genes which are not necessary for parasitic lifestyle or increasing gene copies corresponding to lineage-specific biological processes.Okinawa Institute of Science and Technology Graduate Universit