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Comparative Characterization of Mitogenomes From Five Orders of Cestodes (Eucestoda: Tapeworms).

ABSTRACT: The recognized potential of using mitogenomics in phylogenetics and the more accessible use of high-throughput sequencing (HTS) offer an opportunity to investigate groups of neglected organisms. Here, we leveraged HTS to execute the most comprehensive documentation of mitogenomes for cestodes based on the number of terminals sequenced. We adopted modern approaches to obtain the complete mitogenome sequences of 86 specimens representing five orders of cestodes (three reported for the first time: Phyllobothriidea, "Tetraphyllidea" and Trypanorhyncha). These complete mitogenomes represent an increase of 41% of the mitogenomes available for cestodes (61-147) and an addition of 33% in the representativeness of the cestode orders. The complete mitochondrial genomes are conserved, circular, encoded in the same strand, and transcribed in the same direction, following the pattern observed previously for tapeworms. Their length varies from 13,369 to 13,795 bp, containing 36 genes in total. Except for the Trypanorhyncha specimen, the gene order of the other four cestode orders sequenced here suggests that it could be a synapomorphy for the acetabulate group (with a reversion for taenids). Our results also suggest that no single gene can tell all the evolutionary history contained in the mitogenome. Therefore, cestodes phylogenies based on a single mitochondrial marker may fail to capture their evolutionary history. We predict that such phylogenies would be improved if conducted under a total evidence framework. The characterization of the new mitochondrial genomes is the first step to provide a valuable resource for future studies on the evolutionary relationships of these groups of parasites.

SUBMITTER: Trevisan B

PROVIDER: S-EPMC8727539 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundMitochondrial genomes comprise a small but critical component of the total DNA in eukaryotic organisms. They encode several key proteins for the cell's major energy producing apparatus, the mitochondrial respiratory chain. Additionally, their nucleotide and amino acid sequences are of great utility as markers for systematics, molecular ecology and forensics. Their characterization through nucleotide sequencing is a fundamental starting point in mitogenomics. Methods to amplify complete mitochondrial genomes rapidly and efficiently from microgram quantities of tissue of single individuals are, however, not always available. Here we validate two approaches, which combine long-PCR with Roche 454 pyrosequencing technology, to obtain two complete mitochondrial genomes from individual amphibian species.ResultsWe obtained two new xenopus frogs (Xenopus borealis and X. victorianus) complete mitochondrial genome sequences by means of long-PCR followed by 454 of individual genomes (approach 1) or of multiple pooled genomes (approach 2), the mean depth of coverage per nucleotide was 9823 and 186, respectively. We also characterised and compared the new mitogenomes against their sister taxa; X. laevis and Silurana tropicalis, two of the most intensely studied amphibians. Our results demonstrate how our approaches can be used to obtain complete amphibian mitogenomes with depths of coverage that far surpass traditional primer-walking strategies, at either the same cost or less. Our results also demonstrate: that the size, gene content and order are the same among xenopus mitogenomes and that S. tropicalis form a separate clade to the other xenopus, among which X. laevis and X. victorianus were most closely related. Nucleotide and amino acid diversity was found to vary across the xenopus mitogenomes, with the greatest diversity observed in the Complex 1 gene nad4l and the least diversity observed in Complex 4 genes (cox1-3). All protein-coding genes were shown to be under strong negative (purifying selection), with genes under the strongest pressure (Complex 4) also being the most highly expressed, highlighting their potentially crucial functions in the mitochondrial respiratory chain.ConclusionsNext generation sequencing of long-PCR amplicons using single taxon or multi-taxon approaches enabled two new species of Xenopus mtDNA to be fully characterized. We anticipate our complete mitochondrial genome amplification methods to be applicable to other amphibians, helpful for identifying the most appropriate markers for differentiating species, populations and resolving phylogenies, a pressing need since amphibians are undergoing drastic global decline. Our mtDNAs also provide templates for conserved primer design and the assembly of RNA and DNA reads following high throughput "omic" techniques such as RNA- and ChIP-seq. These could help us better understand how processes such mitochondrial replication and gene expression influence xenopus growth and development, as well as how they evolved and are regulated.

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Comparative Characterization of Mitogenomes From Five Orders of Cestodes (Eucestoda: Tapeworms).

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