The myxozoan minicollagen gene repertoire was not simplified by the parasitic lifestyle: Computational identification of a novel myxozoan minicollagen gene
- Background: Lineage-specific gene expansions represent one of the driving forces in the evolutionary dynamics of unique phylum traits. - Phylogenetic analyses support a close relationship between myxozoan Ncol- 1 – 3 with minicollagens of Polypodium hydriforme, but suggest independent evolution in the case of the myxozoan minicollagens Ncol-4 and Ncol-5. - 1 Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, Ceske Budejovice, Czech Republic. - The process of attachment of a myxozoan spore to the host is mediated by eversion of the polar tubules, which are coiled in highly complex organelles called polar cap- sules. - After nematocyte maturation, minicollagens are modified and anchored on the inner side of the wall in the form of highly com- pacted molecular structures . - Conversely, the discovery of the fourth myx- ozoan minicollagen type suggested a higher polar capsule gene complexity [22]. - Nevertheless, the disparity in pro- tein contents assumed an alternative explanation with high homogeneity of the polar capsule [23].. - The proteomic composition of the. - Reconstruction of the evolutionary history of minicol- lagens is limited by the structural constraints on se- quence variation, as well as by extensive repetitive elements. - This is an example of the common phenomenon of parasitic co-infections in the same host.. - A schematic repre- sentation of the de novo transcriptome reconstruction pipe- line is shown in Fig. - Raw reads of both transcriptomes isolated from the urinary bladder and kidney of pike revealed host contamination, and the only transcriptome of the sporo- gonic stages of M. - we detected the presence of the SSU rDNA gene of N. - The remaining unmapped reads of the M. - PCR also supported the absence of the conserved terminal KR dipeptide motif in the pro- peptide sequence.. - Three-dimensional (3D) structural homology analyses of the N-terminal CRD of newly identified Ncol-5 of M.. - vulgaris, as supported by accuracy testing of the superimposed structures.. - Lack of alanine in the fifth repeat of the Gly-X-Y, is replaced by the gly- cine residue [22] in a modified polyproline domain. - Phylogenetic reconstruction of the cnidarian minicol- lagens suffers from very low nodal supports and unstable topologies at lower (i.e., more ancient) nodes of the phylogenetic tree (Fig. - Myxozoan Ncol-5 is structurally similar to myxozoan Ncol-1 and Ncol-3 in terms of the size of the central Gly-X-Y (colla- gen) domain region, which is surrounded by single CRDs at both ends. - Similar modifications of the polypro- line domain can also be found in other cnidarians.. - 4 Schematic illustration of the myxozoan minicollagen position in the genome. - Reconstruction of the evolutionary history and phylo- genetic relationships of the minicollagen gene family is challenging. - Nonetheless, we observed a high degree of instability in the phylogenetic trees as a consequence of the low phylogenetic signal of these protein-coding genes. - Our BI analysis also revealed a close relation- ship between myxozoan Ncol-5 and Polypodium Ncol- 10, which strengthens the idea of a common evolution- ary history of the Myxozoa and P. - The evolutionary reconstruction indicated that the 21 known minicollagen types reported in Hydra [24] are a result of recent evolutionary multiplication of ancestral types of the minicollagen, in various clusters.. - Only a single nematocyst type has been reported in Myxozoa, and this may explain the limited multiplication of the minicollagen types within the myxozoan minicollagen gene repertoire (only one duplication in S. - Alternatively, the absence of this missing myxozoan minicollagen may be the result of gene loss over the course of evolution of the parasitic lifestyle of myxozoans.. - pickii provides novel transcriptomic data of myxozoan extrasporogonial stages during which extensive proliferation of the parasite is typical, and spore formation is never observed [31, 35].. - pickii fill the cytoplasm of endothelial cells of the host glomerular capillary and thus represent an atypical myxozoan xenoma-like intracellular development stage. - We detected two minicollagen genes, Ncol-3 and Ncol-5, in the transcriptome of the xenoma stage of N. - lieberkuehni supported the SSU rDNA-based analysis in [35], which proved the nonconspecificity of the pike para- sites M. - [41] reported a contraction of the myxozoan polar tu- bule after its release from the myxozoan polar capsule, causing the spore to move closer to the host surface for entry of the infective sporoplasm. - The glycine/glutamine-rich domain is part of the elastic protein Cnidoin, which was discovered in the proteome of Hydra nematocysts [24]. - its elastic sequence is homologous to the glycine-rich region of the spider silk protein Spidroin-2 [42]. - Remarkably, the cysteine pattern (C…C...C….C…..CC) of the C- terminal CRDs of Ncol-4 and Ncol-5 in the 9/10 residue spacing between C2 and C3 represents a common struc- tural motif. - We assume, based on specific aspects of the gene structure, that Ncol-5 may play a specific role in the function of the polar capsule or tubule development. - Our reconstruction of the mini- collagen evolutionary history also suggests recent gene multiplications in Cnidaria, and indicates that myxozoan minicollagen repertoires have not been simplified by. - Moreover, our novel bioinformatic pipeline improved by the filtering step of the coinfection by closely related species in transcriptome assembly will be a useful resource for such generations of transcrip- tomes in the future.. - Myxozoan sampling and extraction of DNA and RNA Ten individuals of the Northern pike E. - Assembly of the transcriptome of M. - To specify the mining procedure, we filtered out specific regions, including N and C-terminal regions of the CRD domains of each minicollagen group.. - For each search of the minicollagen protein group, an E-value threshold of 1e − 5 was adopted. - The SignalP 4.1 web tool was used to determine the presence and location of the signal peptide and putative cleavage sites [52]. - published NMR structure of the Cys-rich N-terminal do- main of H. - Purification and sequencing of the PCR products were performed as described above.. - org/10.1186/s . - ASH advised the project and contributed to the drafting of the manuscript. - All authors read, commented on, and approved the final version of the manuscript.. - 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