A novel minicollagen gene links cnidarians and myxozoans

Abstract

Myxozoans are enigmatic endoparasitic organisms sharing morphological features with bilateria, protists and cnidarians. This, coupled with their highly divergent gene sequences, has greatly obscured their phylogenetic affinities. Here we report the sequencing and characterization of a minicollagen homologue (designated Tb-Ncol-1) in the myxozoan Tetracapsuloides bryosalmonae. Minicollagens are phylum-specific genes encoding cnidarian nematocyst proteins. Sequence analysis revealed a cysteine-rich domain (CRD) architecture and genomic organization similar to group 1 minicollagens. Homology modelling predicted similar three-dimensional structures to Hydra CRDs despite deviations from the canonical pattern of group 1 minicollagens. The discovery of this minicollagen gene strongly supports myxozoans as cnidarians that have radiated as endoparasites of freshwater, marine and terrestrial hosts. It also reveals novel protein sequence variation of relevance to understanding the evolution of nematocyst complexity, and indicates a molecular/morphological link between myxozoan polar capsules and cnidarian nematocysts. Our study is the first to illustrate the power of using genes related to a taxon-specific novelty for phylogenetic inference within the Metazoa, and it exemplifies how the evolutionary relationships of other metazoans characterized by extreme sequence divergence could be similarly resolved.

Genomic insights into the evolutionary origin of Myxozoa within Cnidaria

“…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.…”

New phylogenomic and comparative analyses provide corroborating evidence that Myxozoa is Cnidaria

“…Morphologically, all myxozoans possess polar capsules, which are extraordinarily similar to the cnidarian nematocysts in structure and function (Weill, 1938). Molecularly, a homolog to minicollagens, which are cnidarian-specific nematocyst proteins, was detected in the malacosporean T. bryosalmonae (Holland et al, 2010), further indicating a close relationship between myxozoan polar capsules and cnidarian nematocysts. Additionally, an ultrastructure study revealed tetraradially arranged musculature in B. plumatellae consistent with that in medusozoans, indicating an affinity between Myxozoa and Medusozoa within Cnidaria (Gruhl and Okamura, 2012).…”

“…The putative signal peptides were predicted using SignalP version 3.0 software (Bendtsen et al, 2004). The three-dimensional models of the Nand C-terminal cysteine rich domains (CRDs) of the T. kitauei minicollagen homologs were constructed following the homolog modeling procedures described in a previous study (Holland et al, 2010). The candidate genes possessing the sequence characteristics of known minicollagen proteins were considered minicollagen homologs in the T. kitauei genome.…”

“…All known minicollagen proteins were collected from the NCBI protein database and a previous study (Holland et al, 2010). The proteins were aligned and a profile hidden Markov model (HMM) was built with hmmbuild to search against the predicted proteome of T. kitauei with hmmsearch using the HMMER 3.0 software package (Finn et al, 2011).…”

Proteome of Hydra Nematocyst

“…They represent an exclusive feature of cnidarians, and nematocyst proteins like minicollagens serve as a phylogenetic marker for this phylum as exemplified by a recent report on minicollagens in myxosporidians (39). The identification of the nematocyst proteome of Hydra for the first time allows a view into the evolutionary history of this organelle.…”