Diversity and evolution of myxozoan minicollagens and nematogalectins

Myxozoa are a diverse group of metazoan parasites with a very simple organization, which has for decades eluded their evolutionary origin. Their most prominent and characteristic feature is the polar capsule: a complex intracellular structure of the myxozoan spore, which plays a role in host infection. Striking morphological similarities have been found between myxozoan polar capsules and nematocysts, the stinging structures of cnidarians (corals, sea anemones and jellyfish) leading to the suggestion that Myxozoa and Cnidaria share a more recent common ancestry. This hypothesis has recently been supported by phylogenomic evidence and by the identification of a nematocyst specific minicollagen gene in the myxozoan Tetracapsuloides bryosalmonae. Here we searched genomes and transcriptomes of several myxozoan taxa for the presence of additional cnidarian specific genes and characterized these genes within a phylogenetic context.

Illumina assemblies of transcriptome or genome data of three myxozoan species (Enteromyxum leei, Kudoa iwatai, and Sphaeromyxa zaharoni) and of the enigmatic cnidarian parasite Polypodium hydriforme (Polypodiozoa) were mined using tBlastn searches with nematocyst-specific proteins as queries. Several orthologs of nematogalectins and minicollagens were identified. Our phylogenetic analyses indicate that myxozoans possess three distinct minicollagens. We found that the cnidarian repertoire of nematogalectins is more complex than previously thought and we identified additional members of the nematogalectin family. Cnidarians were found to possess four nematogalectin/ nematogalectin-related genes, while in myxozoans only three genes could be identified.

Our results demonstrate that myxozoans possess a diverse array of genes that are taxonomically restricted to Cnidaria. Characterization of these genes provide compelling evidence that polar capsules and nematocysts are homologous structures and that myxozoans are highly degenerate cnidarians. The diversity of minicollagens was higher than previously thought, with the presence of three minicollagen genes in myxozoans. Our phylogenetic results suggest that the different myxozoan sequences are the results of ancient divergences within Cnidaria and not of recent specializations of the polar capsule. For both minicollagen and nematogalectin, our results show that myxozoans possess less gene copies than their cnidarian counter parts, suggesting that the polar capsule gene repertoire was simplified with their reduced body plan.