Dataset Information

Complex mitogenomic rearrangements within the Pectinidae (Mollusca: Bivalvia).

ABSTRACT:

Background

Scallops (Bivalvia: Pectinidae) present extraordinary variance in both mitochondrial genome size, structure and content, even when compared to the extreme diversity documented within Mollusca and Bivalvia. In pectinids, mitogenome rearrangements involve protein coding and rRNA genes along with tRNAs, and different genome organization patterns can be observed even at the level of Tribes. Existing pectinid phylogenies fail to resolve some relationships in the family, Chlamydinae being an especially problematic group.

Results

In our study, we sequenced, annotated and characterized the mitochondrial genome of a member of Chlamydinae, Mimachlamys varia-a species of commercial interest and an effective bioindicator-revealing yet another novel gene arrangement in the Pectinidae. The phylogeny based on all mitochondrial protein coding and rRNA genes suggests the paraphyly of the Mimachlamys genus, further commending the taxonomic revision of the classification within the Chlamydinae subfamily. At the scale of the Pectinidae, we found that 15 sequence blocks are involved in mitogenome rearrangements, which behave as separate units.

Conclusions

Our study reveals incongruities between phylogenies based on mitochondrial protein-coding versus rRNA genes within the Pectinidae, suggesting that locus sampling affects phylogenetic inference at the scale of the family. We also conclude that the available taxon sampling does not allow for understanding of the mechanisms responsible for the high variability of mitogenome architecture observed in the Pectinidae, and that unraveling these processes will require denser taxon sampling.

SUBMITTER: Malkocs T

PROVIDER: S-EPMC8915466 | biostudies-literature | 2022 Mar

REPOSITORIES: biostudies-literature

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Publications

Complex mitogenomic rearrangements within the Pectinidae (Mollusca: Bivalvia).

Malkócs Tamás T Viricel Amélia A Becquet Vanessa V Evin Louise L Dubillot Emmanuel E Pante Eric E

BMC ecology and evolution 20220310 1

<h4>Background</h4>Scallops (Bivalvia: Pectinidae) present extraordinary variance in both mitochondrial genome size, structure and content, even when compared to the extreme diversity documented within Mollusca and Bivalvia. In pectinids, mitogenome rearrangements involve protein coding and rRNA genes along with tRNAs, and different genome organization patterns can be observed even at the level of Tribes. Existing pectinid phylogenies fail to resolve some relationships in the family, Chlamydinae ...[more]

PMID: 35272625

Similar Datasets

Project description:BackgroundIt can be seen from the available mollusk mitogenomes that the family Pectinidae exhibits the most variation in genome organization. In this study, comparative mitogenomic analyses were performed for three scallops from the subfamily Chlamydinae (Pectinidae), with the goal of characterizing the degree of variability of mitogenome organization and other characteristics among species from the same subfamily and exploring their possible evolution route.FindingsThe complete or nearly complete mtDNA sequences of scallop Mimachlamys nobilis (17,935 bp), Mizuhopecten yessoensis (20,964 bp) and Chlamys farreri (17,035 bp) were determined using long PCR amplification and primer walking sequencing strategy. Highly variable size difference of the three genomes resulted primarily from length and number variations of non-coding regions, and the major difference in gene content of the three scallop species are due to varying tRNA gene sets. Only 21, 16, and 17 tRNA genes were detected in the mitogenomes of M. nobilis, M. yessoensis and C. farreri, respectively. Remarkably, no trnS gene could be identified in any of the three scallops. A newly-detected trnA-like sequence within the mitogenome of M. yessoensis seems to exemplify the functional loss of a tRNA gene, and the duplication of trnD in M. yessoensis raises a fundamental question of whether the retention of the tRNA gene copy of 2-tRNAs is easier than that of 4-tRNAs. Analysis of putative evolutionary pathways of gene rearrangement indicates that transposition of neighboring gene blocks may play an important role in the evolution of mitogenomes in scallops. Parsimonious analysis of the genomic variations implies that the mitogenomes of M. yessoensis and C. farreri are likely to derive independently from a common ancestor that was closely related to M. nobilis.ConclusionComparative mitogenomic analyses among three species from the subfamily Chlamydinae show that the three genomes exhibit a high level of genomic variation and a diversity of tRNA gene sets, characterized by extensive translocation of genes. These features provide useful clues and information for evolutionary analysis of scallop mitogenomes.

Project description:BACKGROUND:Doubly uniparental inheritance (DUI) is an atypical system of animal mtDNA inheritance found only in some bivalves. Under DUI, maternally (F genome) and paternally (M genome) transmitted mtDNAs yield two distinct gender-associated mtDNA lineages. The oldest distinct M and F genomes are found in freshwater mussels (order Unionoida). Comparative analyses of unionoid mitochondrial genomes and a robust phylogenetic framework are necessary to elucidate the origin, function and molecular evolutionary consequences of DUI. Herein, F and M genomes from three unionoid species, Venustaconcha ellipsiformis, Pyganodon grandis and Quadrula quadrula have been sequenced. Comparative genomic analyses were carried out on these six genomes along with two F and one M unionoid genomes from GenBank (F and M genomes of Inversidens japanensis and F genome of Lampsilis ornata). RESULTS:Compared to their unionoid F counterparts, the M genomes contain some unique features including a novel localization of the trnH gene, an inversion of the atp8-trnD genes and a unique 3'coding extension of the cytochrome c oxidase subunit II gene. One or more of these unique M genome features could be causally associated with paternal transmission. Unionoid bivalves are characterized by extreme intraspecific sequence divergences between gender-associated mtDNAs with an average of 50% for V. ellipsiformis, 50% for I. japanensis, 51% for P. grandis and 52% for Q. quadrula (uncorrected amino acid p-distances). Phylogenetic analyses of 12 protein-coding genes from 29 bivalve and five outgroup mt genomes robustly indicate bivalve monophyly and the following branching order within the autolamellibranch bivalves: ((Pteriomorphia, Veneroida) Unionoida). CONCLUSION:The basal nature of the Unionoida within the autolamellibranch bivalves and the previously hypothesized single origin of DUI suggest that (1) DUI arose in the ancestral autolamellibranch bivalve lineage and was subsequently lost in multiple descendant lineages and (2) the mitochondrial genome characteristics observed in unionoid bivalves could more closely resemble the DUI ancestral condition. Descriptions and comparisons presented in this paper are fundamental to a more complete understanding regarding the origins and consequences of DUI.

Dataset Information

Complex mitogenomic rearrangements within the Pectinidae (Mollusca: Bivalvia).

Background

Results

Conclusions

Publications

Complex mitogenomic rearrangements within the Pectinidae (Mollusca: Bivalvia).

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