Diversity and evolution of myxozoan minicollagens and nematogalectins

Abstract

BackgroundMyxozoa 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.ResultsIllumina 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-014-0205-0) contains supplementary material, which is available to authorized users.

Genomic insights into the evolutionary origin of Myxozoa within Cnidaria

“…These results are consistent with those of other molecular phylogenetic studies (19,23), although these have been criticized as possible artifacts of long-branch attraction (21). The monophyly of Myxozoa + P. hydriforme is also supported by endoparasitism in fish, a unique cell-within-cell developmental stage, possession of a single similar type of nematocyst (19,23), and similarity in minicollagen sequences (28). This phylogenomic pattern suggests that endoparasitism in Cnidaria was a single event that occurred at the base of Myxozoa + P. hydriforme, but that the dramatic reduction in body plan occurred following the divergence of P. hydriforme from myxozoans, as P. hydriforme retains many cnidarian features.…”

“…In recent studies, myxozoans were found to possess the cnidarian-specific minicollagen and nematogalectin genes (24,27,28), each of which has been shown to play important roles in the nematocyst structure in Hydra (29,30). These studies support previous morphology-based assertions that myxozoan polar capsules are homologous to cnidarian nematocysts (4,5,31,32) and thus indirectly suggest a close evolutionary relationship between these two groups.…”

“…Collection of specimens of P. hydriforme, K. iwatai plasmodia, E. leei trophozoites, and S. zaharoni plasmodia for both genomic and transcriptomic purposes was carried out as described in ref. 28 and SI Materials and Methods. Flash-frozen M. cerebralis actinospores were kindly provided by Ron Hedrick (University of California at Davis).…”

“…P. hydriforme gDNA was sheared to a size of 350 bp, and 100 bp paired-end (PE) sequencing was performed on an Illumina HiSEq 2000. Library preparation and Illumina 100-bp PE HiSEq 2000 sequencing of K. iwatai (transcriptome and genome), S. zaharoni (genome), and E. leei (genome) was described (28). In addition to the Illumina HiSeq sequencing, the K. iwatai genomic library was also independently sequenced with an Illumina Genome Analyzer IIx platform, which produced 95,434,687 paired reads (76 bp).…”

“…For the M. cerebralis trancriptome assembly, RNA extraction, library preparation, and sequencing was performed for the P. hydriforme transcriptome as described (28). Library preparations and genome sequencing of P. hydriforme was carried out at the Genome Sequence Facility at the University of Kansas Medical School.…”