Genomic insights into the evolutionary origin of Myxozoa within Cnidaria

Abstract

The Myxozoa comprise over 2,000 species of microscopic obligate parasites that use both invertebrate and vertebrate hosts as part of their life cycle. Although the evolutionary origin of myxozoans has been elusive, a close relationship with cnidarians, a group that includes corals, sea anemones, jellyfish, and hydroids, is supported by some phylogenetic studies and the observation that the distinctive myxozoan structure, the polar capsule, is remarkably similar to the stinging structures (nematocysts) in cnidarians. To gain insight into the extreme evolutionary transition from a free-living cnidarian to a microscopic endoparasite, we analyzed genomic and transcriptomic assemblies from two distantly related myxozoan species, Kudoa iwatai and Myxobolus cerebralis, and compared these to the transcriptome and genome of the less reduced cnidarian parasite, Polypodium hydriforme. A phylogenomic analysis, using for the first time to our knowledge, a taxonomic sampling that represents the breadth of myxozoan diversity, including four newly generated myxozoan assemblies, confirms that myxozoans are cnidarians and are a sister taxon to P. hydriforme. Estimations of genome size reveal that myxozoans have one of the smallest reported animal genomes. Gene enrichment analyses show depletion of expressed genes in categories related to development, cell differentiation, and cell-cell communication. In addition, a search for candidate genes indicates that myxozoans lack key elements of signaling pathways and transcriptional factors important for multicellular development. Our results suggest that the degeneration of the myxozoan body plan from a free-living cnidarian to a microscopic parasitic cnidarian was accompanied by extreme reduction in genome size and gene content.

Keywords: Cnidaria; Myxozoa; Polypodium; genome evolution; parasite.

Fig. 1.

Life cycles of M. cerebralis and P. hydriforme. (A) M. cerebralis alternates its development between a fish (salmonid) host and an annelid (T. tubifex) host. The myxospore is produced in the fish (Right), and the actinospore is produced in the annelid (Left). Both stages consist of just a few cells, including those housing polar capsules. (B) In P. hydriforme, the stolon stage (Top) develops inside the ovaries of its host (acipenceriform fish). Upon host spawning, P. hydriforme emerges from the host’s oocyte (Right), fragments, and lives as a free-living stage with a mouth (Left) before infecting its host.

Fig. 2.

Phylogenetic tree generated from a matrix of 51,940 amino acid positions and 77 taxa using Bayesian inference under the CAT model. Support values are indicated only for nodes that did not received maximal support. Bayesian posterior probabilities/ML bootstrap supports under the PROTGAMMAGTR model are given near the corresponding node. A minus sign (‘‘−’’) indicates that the corresponding node is absent from the ML bootstrap consensus tree.

Fig. S1.

Phylogenetic tree generated from a matrix of 41,237 amino acid positions, which excludes ribosomal genes, and 77 taxa using Bayesian inference under the CAT model. Support values are indicated only for nodes that did not receive maximal support. Bayesian posterior probabilities/ML bootstrap supports under the PROTGAMMAGTR are given near the corresponding node. A minus sign (‘‘–’’) indicates that the corresponding node is absent from the ML bootstrap consensus tree.

Fig. S2.

(A) Phylogenetic tree generated from a matrix of 51,940 amino acid sequences and 30 cnidarian taxa using Bayesian inference under the CAT model. Support values are indicated only for nodes that did not receive maximal support. Bayesian posterior probabilities under the CAT model/Bayesian posterior probabilities under the CAT-GTR model/ML bootstrap supports under the PROTGAMMAGTR are given near the corresponding node. A minus sign (‘‘–’’) indicates that the corresponding node is absent from the ML bootstrap consensus tree. (B) Phylogenetic tree generated from a matrix that excludes ribosomal genes, comprising 41,237 amino acid sequences and 30 cnidarian taxa using Bayesian inference under the CAT model. Support values are indicated only for nodes that did not receive maximal support. Bayesian posterior probabilities/ML bootstrap supports under the PROTGAMMAGTR are given near the corresponding node.

Fig. S3.

Sequence size distribution of the assembled transcriptome sequences.

Fig. 3.

GO annotation of unigenes in transcriptomes. The top 20 GO categories are shown as a percentage of total GO terms from the transcriptome assemblies of M. cerebralis, K. iwatai, P. hydriforme, and the published protein sequences of H. magnipapillata and N. vectensis. Categories for which myxozoans present significantly fewer GO terms than other cnidarians are indicated by boldface type.

Fig. S4.

GO annotation of unigenes in genomes and transcriptomes. The top 20 GO categories are shown as a percentage of total GO terms from the assemblies of K. iwatai, P. hydriforme, and the published protein sequences of H. magnipapillata and N. vectensis. Categories for which K. iwatai presents significantly fewer GO terms than other cnidarians are indicated in boldface type.

Fig. S5.

Comparison of OGs in myxozoan and other cnidarian transcriptomes. VENN diagram comparing OGs for the OrthoMCL database from transcriptome assemblies of K. iwatai and P. hydriforme and published predicted proteins in H. magnipapillata and N. vectensis.