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Eternal morphology of kinorhynchs. A. Pycnophyes kielensis, scale bar = 500 μm; B. Echinoderes svetlanae, scale bar = 200 μm. Heads orient down.
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Many features of mitochondrial genomes of animals, such as patterns of gene arrangement, nucleotide content and substitution rate variation are extensively used in evolutionary and phylogenetic studies. Nearly 6,000 mitochondrial genomes of animals have already been sequenced, covering the majority of animal phyla. One of the groups that escaped mi...
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Background
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Citations
... In S. destruens, trnM1 and trnM3 share a higher nucleotide similarity, 70%, in comparison to trnM2 which is 54% and 63%, respectively. The trnM replication in S. destruens could represent different functions of the methionine tRNAs in protein synthesis and initiation of translation [38]; however, the functional significance remains unknown. ...
Background:
Sphaerothecum destruens is an obligate intracellular fish parasite which has been identified as a serious threat to freshwater fishes. Taxonomically, S. destruens belongs to the order Dermocystida within the class Ichthyosporea (formerly referred to as Mesomycetozoea), which sits at the animal-fungal boundary. Mitochondrial DNA (mtDNA) sequences can be valuable genetic markers for species detection and are increasingly used in environmental DNA (eDNA) based species detection. Furthermore, mtDNA sequences can be used in epidemiological studies by informing detection, strain identification and geographical spread.
Methods:
We amplified the entire mitochondrial (mt) genome of S. destruens in two overlapping long fragments using primers designed based on the cox1, cob and nad5 partial sequences. The mt-genome architecture of S. destruens was then compared to close relatives to gain insights into its evolution.
Results:
The complete mt-genome of Sphaerothecum destruens is 23,939 bp in length and consists of 47 genes including 21 protein-coding genes, 2 rRNA, 22 tRNA and two unidentified open reading frames. The mitochondrial genome of S. destruens is intronless and compact with a few intergenic regions and includes genes that are often missing from animal and fungal mt-genomes, such as, the four ribosomal proteins (small subunit rps13 and 14; large subunit rpl2 and 16), tatC (twin-arginine translocase component C), and ccmC and ccmF (cytochrome c maturation protein ccmC and heme lyase).
Conclusions:
We present the first mt-genome of S. destruens which also represents the first mt-genome for the order Dermocystida. The availability of the mt-genome can assist the detection of S. destruens and closely related parasites in eukaryotic diversity surveys using eDNA and assist epidemiological studies by improving molecular detection and tracking the parasite's spread. Furthermore, as the only representative of the order Dermocystida, its mt-genome can be used in the study of mitochondrial evolution of the unicellular relatives of animals.
... In some lineages, additional tRNA gene copies may be maintained for relatively long periods of time. As an example, two trnM genes were found in the mt genomes of some mantellid and dicroglossid frogs (Kurabayashi et al., 2008;Zhang et al., 2018), Scaridae fishes (Mabuchi et al., 2004), bivalve mollusc lineages (Wu et al., , 2014, terebelliform annelids (Zhong et al., 2008), and kinorhynch worms (Popova et al., 2016); duplicated trnT genes were found in most lineages of ardeid birds (Zhou et al., 2014); and additional trnM and trnR genes were found in almost all Porifera lineages (Lavrov et al., 2012;Maikova et al., 2015;Wang and Lavrov, 2011;Sahyoun et al., 2015). However, a more frequent scenario of duplicated tRNA gene evolution is that in which one of the copies gradually accumulates substitutions and turns into a pseudogene (reviewed in Jühling et al., 2012). ...
The evolution of tRNA genes in mitochondrial (mt) genomes is a complex process that includes duplications, degenerations, and transpositions, as well as a specific process of identity change through mutations in the anticodon (tRNA gene remolding or tRNA gene recruitment). Using amphipod-specific tRNA models for annotation, we show that tRNA duplications are more common in the mt genomes of amphipods than what was revealed by previous annotations. Seventeen cases of tRNA gene duplications were detected in the mt genomes of amphipods, and ten of them were tRNA genes that underwent remolding. The additional tRNA gene findings were verified using phylogenetic analysis and genetic distance analysis. The majority of remolded tRNA genes (seven out of ten cases) were found in the mt genomes of endemic amphipod species from Lake Baikal. All additional mt tRNA genes arose independently in the Baikalian amphipods, indicating the unusual plasticity of tRNA gene evolution in these species assemblages. The possible reasons for the unusual abundance of additional tRNA genes in the mt genomes of Baikalian amphipods are discussed.
The amphipod-specific tRNA models developed for MiTFi refine existing predictions of tRNA genes in amphipods and reveal additional cases of duplicated tRNA genes overlooked by using less specific Metazoa-wide models. The application of these models for mt tRNA gene prediction will be useful for the correct annotation of mt genomes of amphipods and probably other crustaceans.
... The tRNA gene duplication in D. conopsoides is most likely a recent event as it is not present in D. longicornis and other tephritid fruit flies. The functional significance of mitochondrial trnF and trnE genes duplication in D. conopsoides fruit fly is not clear, but it might represent different functions of these genes in protein synthesis and initiation of translation (Popova et al., 2016). ...
To date there is only a single report on the complete mitochondrial genome of the Dacus fruit flies. We report here the whole mitogenome of Dacus conopsoides with first report of tRNA gene duplication in tephritid fruit flies determined using next-generation sequencing and discuss the molecular phylogeny of Dacini tribe. It had a total length of 15,852 bp, comprising 13 protein coding genes, 2 rRNA genes, 23 tRNA genes, and a non-coding region (A + T-rich control region). The 65-bp trnF gene was duplicated, and the 68-bp trnE gene was partially duplicated resulting in a 31-bp pseudogene. The cloverleaf structure for trnN, trnH, and trnF lacked the TΨC-loop, while trnS lacked the D-stem. The start codons for the protein coding genes included 6 ATG, 3 ATC, 2 ATA, and 1 each of ATT and TCG. Seven PCGs had TAA stop codon, two had TAG and four had incomplete T stop codon. Molecular phylogeny based on 15 mt-genes (13 PCGs +2 rRNA genes) and 30 taxa of Tephritidae indicated D. conopsoides forming a monophyletic sister group with D. longicornis supported by high bootstrap value. The lineage containing also the monophyletic genus Zeugodacus. The Dacini and Ceratitidini tribes of the subfamily Dacinae were monophyletic but the subfamilies Dacinae and Trypetinae were paraphyletic. A broader taxa sampling of the Tephritidae is needed to better elucidate the phylogenetics and systematics of the tribes and subfamilies of tephritid fruit flies.
... Recent sequencing technologies have permitted more in-depth investigations of meiofaunal organisms, but scalidophorans remain genetically understudied relative to other ecdysozoans. Kinorhynchs have few genetic resources available; beyond barcoding, two mitochondrial genomes (Popova et al. 2016) are joined by a single 454 transcriptome that is relatively incomplete (Borner et al. 2014). Even with a single high-quality transcriptome certain genes, notably opsins, were not recovered conclusively. ...
A new kinorhynch species, Echinoderes kohni sp. nov., is described from the San Juan Archipelago, northwest Washington State, USA. The species’ spine/tube distribution combined with the presence of long, spiniform tergal extensions assign it to the Echinoderes spinifurca species group. It is distinguished from other species in the group by its enlarged fringe tips on the posterior sternal plate margins of segment 10, and by its distribution of type 2 glandular cell outlets and sensory spots. Together with the morphological description we provide a de novo assembled transcriptome for the species, generated from a single individual. This represents the first time a kinorhynch has been described together with genetic data beyond a barcode.
... Virtually all subsequent phylogenomic analyses have found support for Ecdysozoa (e.g., Philippe et al. 2005;Irimia et al. 2007;Dunn et al. 2008;Hejnol et al. 2009). That is not however the case from mitogenomics (Podsiadlowski et al. 2008;Rota-Stabelli et al. 2010;Popova et al. 2016), but as of today, no mitochondrial genomes are available for Nematomorpha or Loricifera-and some loriciferans may altogether lack mitochondria (Danovaro et al. 2010;Danovaro et al. 2016). ...
... Little is known about kinorhynch nuclear genomes, with no size estimate or sequence currently available. Only recently two mitochondrial genomes have been published (Popova et al. 2016)-Echinoderes svetlanae (Cyclorhagida) and Pycnophyes kielensis (Allomalorhagida). Their mitochondrial genomes are circular molecules approximately 15 Kb in size, with the typical metazoan complement of 37 genes, which are all positioned on the major strand, but the gene order is distinct and unique among Ecdysozoa (Popova et al. 2016), including duplicated methionine tRNA genes. ...
... Only recently two mitochondrial genomes have been published (Popova et al. 2016)-Echinoderes svetlanae (Cyclorhagida) and Pycnophyes kielensis (Allomalorhagida). Their mitochondrial genomes are circular molecules approximately 15 Kb in size, with the typical metazoan complement of 37 genes, which are all positioned on the major strand, but the gene order is distinct and unique among Ecdysozoa (Popova et al. 2016), including duplicated methionine tRNA genes. ...
Twenty years after its proposal, the monophyly of molting protostomes-Ecdysozoa-is a well-corroborated hypothesis, but the interrelationships of its major subclades are more ambiguous than is commonly appreciated. Morphological and molecular support for arthropods, onychophorans and tardigrades as a clade (Panarthropoda) continues to be challenged by a grouping of tardigrades with Nematoida in some molecular analyses, although onychophorans are consistently recovered as the sister group of arthropods. The status of Cycloneuralia and Scalidophora, each proposed by morphologists in the 1990s and widely employed in textbooks, is in flux: Cycloneuralia is typically non-monophyletic in molecular analyses, and Scalidophora is either contradicted or incompletely tested because of limited genomic and transcriptomic data for Loricifera, Kinorhyncha, and Priapulida. However, novel genomic data across Ecdysozoa should soon be available to tackle these difficult phylogenetic questions. The Cambrian fossil record indicates crown-group members of various ecdysozoan phyla as well as stem-group taxa that assist with reconstructing the most recent common ancestor of panarthropods and cycloneuralians.
The kinorhynch species Echinoderes remanei (Blake, 1930) is redescribed herein, based on the material housed in the National Museum of Natural History, Smithsonian Institution in Washington D.C as well as specimens collected at several other sites in the Northern Hemisphere. E. remanei is characterized by the presence of middorsal spines on segments 4 to 8 and lateroventral spines on segments 6 to 9; four pairs of glandular cell outlets type 2 on segment 2 (subdorsal, laterodorsal, sublateral, and ventrolateral), and one pair on segment 4 (subdorsal), 5 (midlateral), 8 (sublateral) and 10 (laterodorsal); lateroventral tubes on segment 5; and by sexual dimorphism expressed in lateral terminal spine lengths (in females, the lateral terminal spines are on about half as long as those in males). The study also reveals that the two other species, Echinoderes tubilak Higgins & Kristensen, 1988 and Echinoderes svetlanae Adrianov, 1999 in Adrianov & Malakhov (1999) are conspecific with E. remanei. Therefore, E. tubilak and E. svetlanae are proposed as junior synonyms of E. remanei and are synonymized with E. remanei (Blake, 1930).
In contrast to highly conserved mitogenomic architecture in most metazoan lineages, which indicates that rearrangement events are generally strongly selected against, a limited number of often unrelated lineages exhibit highly elevated architectural evolution rates. The underlying reasons for this discontinuity in the mitogenomic evolution remain unknown. Previously we sequenced the mitochondrial genome of the first Camallanoidea species, Camallanus cotti (Nematoda: Chromadorea: Spirurina: Camallanidae), and found that it exhibited a highly disrupted architecture. We hypothesised that disrupted architecture might be a synapomorphic feature of the sister-clades Camallanoidea and Dracunculoidea. In this study, we sequenced mitogenomes of three freshwater fish-parasitic nematodes: Camallanus lacustris (Camallanidae), and two Philometridae (Dracunculoidea) species, Clavinema parasiluri, and Philometra sp. In partial agreement with the working hypothesis, both Camallanoidea species had exceptionally large mitogenomes of 18 to 19 Kbp, albeit the underlying reasons differed: in C. lacustris it was the existence of a single enlarged noncoding region of ≈5.5 Kbp. A segment of this region exhibited an inverted base composition skew, which is indicative of a sequence inversion or recombination event. Camallanidae is the second identified chromadorean (first for Spirurina) family that exhibits within-family protein-coding gene rearrangements, and the absence of trnL1 and trnF may be a synapomorphy for Camallanoidea. The underlying reason for the disrupted architecture of Camallanidae does not appear to be a particular event shared by their common ancestor, but rather an underlying mechanism that makes disruptive events more likely in this lineage. In disagreement with the working hypothesis, Spiruromorpha and Oxyuridomorpha exhibited even more highly rearranged gene orders and greater overall branch lengths than Camallanomorpha. However, within-infraorder architecture was highly conserved and leaf nodes very short. This indicates that common ancestors of Spiruromorpha and Oxyuridomorpha clades underwent a period of rapid mitochondrial evolution (both sequence and architecture), followed by a stabilisation after the taxonomic radiation. In contrast to this, Camallanomorpha, and particularly Camallanidae, appear to have entered a period of elevated evolutionary rates after the initial radiations of these two taxa. As a result of this evolutionary discontinuity, there was a strong correlation between the gene order rearrangement rate (GORR) and the overall branch length (0.81), but there was no correlation between the strength of purifying selection (ω=dN/dS) and the overall branch lengths (-0.05) and GORR (-0.04). These findings have important repercussions for future phylogenetic and other evolutionary studies of Spirurina.
The data presented here are related to the research article entitled "Hidden cases of tRNA genes duplication and remolding in mitochondrial genomes of amphipods" (Romanova et al., 2020) [1]. Correct tRNA gene sequence annotation in mitochondrial (mt) and nuclear genomes sometimes can be a challenging task because of the differential performances of tRNA annotation/prediction programmes. These programmes may cause false positive or false negative predictions. Moreover, additional difficulties with annotation may be caused by the presence of duplicated tRNA genes and those coding tRNAs with altered identities occurring as due to a mutation in their anticodon sequence (tRNA gene remolding/recruitment). We developed an R script automating the diagnosis of ancestor tRNA gene coding specificity regardless of anticodon sequence based on genetic distance comparison. Some of the predicted tRNA genes from the mt genomes of amphipods are presented. We also developed an R script for estimation of the best mode of sequence alignment, which was applied to determine the best alignment of tRNA genes in [1], but is also suitable for testing of any nucleotide alignment sets used in phylogenetic inferences.
