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Extensive gene rearrangements in the mitogenomes of congeneric annelid species and insights on the evolutionary history of the genus Ophryotrocha.

ABSTRACT: BACKGROUND:Annelids are one the most speciose and ecologically diverse groups of metazoans. Although a significant effort has been recently invested in sequencing genomes of a wide array of metazoans, many orders and families within the phylum Annelida are still represented by a single specimen of a single species. The genus of interstitial annelids Ophryotrocha (Dorvilleidae, Errantia, Annelida) is among these neglected groups, despite its extensive use as model organism in numerous studies on the evolution of life history, physiological and ecological traits. To compensate for the paucity of genomic information in this genus, we here obtained novel complete mitochondrial genomes of six Ophryotrocha species using next generation sequencing. In addition, we investigated the evolution of the reproductive mode in the Ophryotrocha genus using a phylogeny based on two mitochondrial markers (COXI and 16S rDNA) and one nuclear fragment (Histone H3). RESULTS:Surprisingly, gene order was not conserved among the six Ophryotrocha species investigated, and varied greatly as compared to those found in other annelid species within the class Errantia. The mitogenome phylogeny for the six Ophryotrocha species displayed a separation of gonochoric and hermaphroditic species. However, this separation was not observed in the phylogeny based on the COX1, 16S rDNA, and H3 genes. Parsimony and Bayesian ancestral trait reconstruction indicated that gonochorism was the most parsimonious ancestral reproductive mode in Ophryotrocha spp. CONCLUSIONS:Our results highlight the remarkably high level of gene order variation among congeneric species, even in annelids. This encourages the need for additional mitogenome sequencing of annelid taxa in order to properly understand its mtDNA evolution, high biodiversity and phylogenetic relationships.

SUBMITTER: Tempestini A

PROVIDER: S-EPMC7682095 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Extensive gene rearrangements in the mitogenomes of congeneric annelid species and insights on the evolutionary history of the genus Ophryotrocha.

Tempestini Astrid A Massamba-N'Siala Gloria G Vermandele Fanny F Beaudreau Nicholas N Mortz Mathieu M Dufresne France F Calosi Piero P

BMC genomics 20201123 1

<h4>Background</h4>Annelids are one the most speciose and ecologically diverse groups of metazoans. Although a significant effort has been recently invested in sequencing genomes of a wide array of metazoans, many orders and families within the phylum Annelida are still represented by a single specimen of a single species. The genus of interstitial annelids Ophryotrocha (Dorvilleidae, Errantia, Annelida) is among these neglected groups, despite its extensive use as model organism in numerous stu ...[more]

PMID: 33225885

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Project description:BackgroundComplete mitochondrial (mt) genomes have been sequenced for thousands of animals and represent a molecule of choice for many evolutionary studies. Nevertheless, some animal groups have remained under-sampled. Ctenophora (comb jellies) is one such example, with only two complete mt sequences determined hitherto for this phylum, which encompasses ca. 150-200 described species. This lack of data derives from the extremely fast mt evolutionary rate in this lineage, complicating primer design and DNA amplification. Indeed, in the two ctenophore mt genomes sequenced to date, i.e. those of Mnemiopsis leidyi (order Lobata) and Pleurobrachia bachei (order Cydippida), both rRNA and protein coding genes exhibit an extraordinary size reduction and have highly derived sequences. Additionally, all tRNAs, and the atp6 and atp8 genes are absent. In order to determine whether these characteristics are shared by other ctenophores, we obtained the complete mt genomes of three benthic ctenophores belonging to the so far unsampled order of Platyctenida: Coeloplana loyai, Coeloplana yulianicorum and Vallicula multiformis.ResultsThe mt genomes of benthic ctenophores reveal the same peculiarities found in Mnemiopsis and Pleurobrachia, demonstrating that the fast evolutionary rate is a general trait of the ctenophore mt genomes. Our results also indicate that this high evolutionary rate not only affects the nucleotide substitution but also gene rearrangements. Indeed, gene order was highly rearranged among representatives of the different taxonomic orders in which it was close to random, but also quite variable within Platyctenida, in which the genera Coeloplana and Vallicula share only four conserved synteny blocks. However, the two congeneric Coeloplana species display exactly the same gene order. Because of the extreme evolutionary rate, our phylogenetic analyses were unable to resolve the phylogenetic position of ctenophores within metazoans or the relationships among the different Ctenophora orders. Comparative sequence-analyses allowed us to correct the annotation of the Pleurobrachia mt genome, confirming the absence of tRNAs, the presence of both rRNA genes, and the existence of a reassignment of codon TGA from tryptophan to serine for this species.ConclusionsSince Platyctenida is an early diverging lineage among Ctenophora, our findings suggest that the mt traits described above are ancestral characteristics of this phylum.

Dataset Information

Extensive gene rearrangements in the mitogenomes of congeneric annelid species and insights on the evolutionary history of the genus Ophryotrocha.

Publications

Extensive gene rearrangements in the mitogenomes of congeneric annelid species and insights on the evolutionary history of the genus Ophryotrocha.

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