Abstract
Among invertebrates, only a few groups still have uncertain phylogenetic position, Orthonectida, a small group of rare multi-cellular parasites of marine invertebrates, being one of them. Recent molecular and morphological findings suggest that orthonectids belong to Lophotrochozoa and are close to Annelida. Nevertheless, phylogenetic relationships between orthonectids and annelids are unclear, and the phylogeny within the group itself has never been studied. Sequencing of mitochondrial genomes is used here to clarify this issue. Complete mt genomes of the orthonectids Intoshia variabili and Rhopalura litoralis were characterized and compared with Intoshia linei mt genome. Our results show that Orthonectida mt genomes have undergone reduction and gene loss, and that they have complicated organization revealed in strand asymmetry in nucleotide composition, in some features of intergenic non-coding regions, tRNA duplication and folding. Moreover, all species of Orthonectida have a unique gene order with complicated rearrangement landscape. Significant differences in mitochondrial genomes in the three orthonectid species could be explained by the fact that their host species belong to different taxa (flat worms, nemertines and gastropods). Among the analyzed mt genomes of Orthonectida, I. linei possesses the closest gene order to the ancestral genome. All Orthonectida species are monophyletic, and in the phylogenetic tree are close to Pleistoannelida, and specifically, to Clitellata.
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Abbreviations
- cox1, cox2, cox3 :
-
Cytochrome oxidase subunit I, II, and III protein genes
- cob :
-
Cytochrome b gene
- atp6, atp8 :
-
ATP synthase subunit 6 and 8 gene
- nad2, nad4, nad4L, nad5, nad6, nad11 :
-
NADH dehydrogenase subunit 1–6, 11 and 4L genes
- \(tRN{A^{Trp}}\), tRNA Ile, RNA Lys, tRNA Met, tRNA Val, tRNA Cys, tRNA Met, tRNA Gln, tRNA Leu1, tRNA Leu2, tRNA Phe, tRNA Arg, tRNA Tyr, tRNA Ser1, tRNA Ser2, tRNA Asp1, tRNA Asp2, tRNA Asn :
-
Transfer RNA genes
- rrnL, rrnS :
-
Ribosomal RNA genes
- ORF:
-
Open reading frames
- PCG:
-
Protein-coding gene
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Acknowledgements
We are thankful to Dr. M. Makarov for providing accommodation and facilities for field work at the Barentz Sea, and also to the staff of the Marine Biological Station of the Saint Petersburg State University for assistance in collecting material. The work was supported by Grant of Russian Foundation for Basic Research (RFBR) no. 19-04-0021 and Saint Petersburg State University research Grant 1.40.496.2017. Bioinformatics was supported with Russian Science Foundation 17-74-10103 Grant to Natalya Bondarenko. This study utilized equipment of the “Centre Biobank” and “Computing Centre SPbU” of Saint Petersburg State University.
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Communicated by B. Franz Lang.
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Bondarenko, N., Bondarenko, A., Starunov, V. et al. Comparative analysis of the mitochondrial genomes of Orthonectida: insights into the evolution of an invertebrate parasite species. Mol Genet Genomics 294, 715–727 (2019). https://doi.org/10.1007/s00438-019-01543-1
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DOI: https://doi.org/10.1007/s00438-019-01543-1