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Diversity and evolution of myxozoan minicollagens and nematogalectins.

Shpirer E, Chang ES, Diamant A, Rubinstein N, Cartwright P, Huchon D - BMC Evol. Biol. (2014)

Bottom Line: Cnidarians were found to possess four nematogalectin/ nematogalectin-related genes, while in myxozoans only three genes could be identified.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, Tel Aviv University, Tel Aviv, Israel. pcart@ku.edu.

ABSTRACT

Background: 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.

Results: 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.

Conclusions: 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.

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Schematic drawing ofKudoanematogalectin and nematogalectin-related proteins. Green: signal peptide; purple: highly conserved areas among nematogalectin of the same type; red: collagen-like domain; blue: gal-lectin-like domain; orange line and triangle: intron-exon boundary.
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Fig5: Schematic drawing ofKudoanematogalectin and nematogalectin-related proteins. Green: signal peptide; purple: highly conserved areas among nematogalectin of the same type; red: collagen-like domain; blue: gal-lectin-like domain; orange line and triangle: intron-exon boundary.

Mentions: Among nematogalectin-related genes, the myxozoan sequences (Figure 4, Additional file 1) possess a similar intron/exon structure as in other cnidarians [27] with a first intron after the end of the signal peptide and a second intron between the collagen and the gal-lectin domains (Figure 5). These two introns are also present in nematogalectin A and nematogalectin C (Additional file 1). The nematogalectins A of Kudoa and Sphaeromyxa possess an additional intron located at the end of the gal-lectin domain, while the nematogalectins C also possess at least five additional introns in their long 5′-region (Additional file 1). No evidence of alternative splicing was found in the CDS of the nematogalectin A, B and the nematogalectin-related genes of Kudoa or Polypodium. However, although it is possible that alternative splicing occurs in the long 5′-region of nematogalectin C of Kudoa, as two different transcripts were found, this could not be confirmed.Figure 5


Diversity and evolution of myxozoan minicollagens and nematogalectins.

Shpirer E, Chang ES, Diamant A, Rubinstein N, Cartwright P, Huchon D - BMC Evol. Biol. (2014)

Schematic drawing ofKudoanematogalectin and nematogalectin-related proteins. Green: signal peptide; purple: highly conserved areas among nematogalectin of the same type; red: collagen-like domain; blue: gal-lectin-like domain; orange line and triangle: intron-exon boundary.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4195985&req=5

Fig5: Schematic drawing ofKudoanematogalectin and nematogalectin-related proteins. Green: signal peptide; purple: highly conserved areas among nematogalectin of the same type; red: collagen-like domain; blue: gal-lectin-like domain; orange line and triangle: intron-exon boundary.
Mentions: Among nematogalectin-related genes, the myxozoan sequences (Figure 4, Additional file 1) possess a similar intron/exon structure as in other cnidarians [27] with a first intron after the end of the signal peptide and a second intron between the collagen and the gal-lectin domains (Figure 5). These two introns are also present in nematogalectin A and nematogalectin C (Additional file 1). The nematogalectins A of Kudoa and Sphaeromyxa possess an additional intron located at the end of the gal-lectin domain, while the nematogalectins C also possess at least five additional introns in their long 5′-region (Additional file 1). No evidence of alternative splicing was found in the CDS of the nematogalectin A, B and the nematogalectin-related genes of Kudoa or Polypodium. However, although it is possible that alternative splicing occurs in the long 5′-region of nematogalectin C of Kudoa, as two different transcripts were found, this could not be confirmed.Figure 5

Bottom Line: Cnidarians were found to possess four nematogalectin/ nematogalectin-related genes, while in myxozoans only three genes could be identified.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, Tel Aviv University, Tel Aviv, Israel. pcart@ku.edu.

ABSTRACT

Background: 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.

Results: 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.

Conclusions: 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.

Show MeSH
Related in: MedlinePlus