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The complete mitochondrial genomes of six heterodont bivalves (Tellinoidea and Solenoidea): variable gene arrangements and phylogenetic implications.

ABSTRACT: BACKGROUND: Taxonomy and phylogeny of subclass Heterodonta including Tellinoidea are long-debated issues and a complete agreement has not been reached yet. Mitochondrial (mt) genomes have been proved to be a powerful tool in resolving phylogenetic relationship. However, to date, only ten complete mitochondrial genomes of Heterodonta, which is by far the most diverse major group of Bivalvia, have been determined. In this paper, we newly sequenced the complete mt genomes of six species belonging to Heterodonta in order to resolve some problematical relationships among this subclass. PRINCIPAL FINDINGS: The complete mt genomes of six species vary in size from 16,352 bp to 18,182. Hairpin-like secondary structures are found in the largest non-coding regions of six freshly sequenced mt genomes, five of which contain tandem repeats. It is noteworthy that two species belonging to the same genus show different gene arrangements with three translocations. The phylogenetic analysis of Heterodonta indicates that Sinonovacula constricta, distant from the Solecurtidae belonging to Tellinoidea, is as a sister group with Solen grandis of family Solenidae. Besides, all five species of Tellinoidea cluster together, while Sanguinolaria diphos has closer relationship with Solecurtus divaricatus, Moerella iridescens and Semele scaba rather than with Sanguinolaria olivacea. CONCLUSIONS/SIGNIFICANCE: By comparative study of gene order rearrangements and phylogenetic relationships of the five species belonging to Tellinoidea, our results support that comparisons of mt gene order rearrangements, to some extent, are a useful tool for phylogenetic studies. Based on phylogenetic analyses of multiple protein-coding genes, we prefer classifying the genus Sinonovacula within the superfamily Solenoidea and not the superfamily Tellinoidea. Besides, both gene order and sequence data agree that Sanguinolaria (Psammobiidae) is not monophyletic. Nevertheless, more studies based on more mt genomes via combination of gene order and phylogenetic analysis are needed to further understand the phylogenetic relationships in subclass Heterodonta.

SUBMITTER: Yuan Y

PROVIDER: S-EPMC3285693 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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The complete mitochondrial genomes of six heterodont bivalves (Tellinoidea and Solenoidea): variable gene arrangements and phylogenetic implications.

Yuan Yang Y Li Qi Q Yu Hong H Kong Lingfeng L

PloS one 20120223 2

<h4>Background</h4>Taxonomy and phylogeny of subclass Heterodonta including Tellinoidea are long-debated issues and a complete agreement has not been reached yet. Mitochondrial (mt) genomes have been proved to be a powerful tool in resolving phylogenetic relationship. However, to date, only ten complete mitochondrial genomes of Heterodonta, which is by far the most diverse major group of Bivalvia, have been determined. In this paper, we newly sequenced the complete mt genomes of six species belo ...[more]

PMID: 22384227

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Project description:BackgroundAlthough recent studies have greatly advanced understanding of deep molluscan phylogeny, placement of some taxa remains uncertain as different datasets support competing class-relationships. Traditionally, morphologists have placed Monoplacophora, a group of morphologically simple, limpet-like molluscs as sister group to all other conchiferans (shelled molluscs other than Polyplacophora), a grouping that is supported by the latest large-scale phylogenomic study that includes Laevipilina. However, molecular datasets dominated by nuclear ribosomal genes support Monoplacophora + Polyplacophora (Serialia). Here, we evaluate the potential of mitochondrial genome data for resolving placement of Monoplacophora.ResultsTwo complete (Laevipilina antarctica and Vema ewingi) and one partial (Laevipilina hyalina) mitochondrial genomes were sequenced, assembled, and compared. All three genomes show a highly similar architecture including an unusually high number of non-coding regions. Comparison of monoplacophoran gene order shows a gene arrangement pattern not previously reported; there is an inversion of one large gene cluster. Our reanalyses of recently published polyplacophoran mitogenomes show, however, that this feature is also present in some chiton species. Maximum Likelihood and Bayesian Inference analyses of 13 mitochondrial protein-coding genes failed to robustly place Monoplacophora and hypothesis testing could not reject any of the evaluated placements of Monoplacophora.ConclusionsUnder both serialian or aculiferan-conchiferan scenarios, the observed gene cluster inversion appears to be a convergent evolution of gene arrangements in molluscs. Our phylogenetic results are inconclusive and sensitive to taxon sampling. Aculifera (Polyplacophora + Aplacophora) and Conchifera were never recovered. However, some analyses recovered Serialia (Monoplacophora + Polyplacophora), Diasoma (Bivalvia + Scaphopoda) or Pleistomollusca (Bivalvia + Gastropoda). Although we could not shed light on deep evolutionary traits of Mollusca we found unique patterns of gene arrangements that are common to monoplacophoran and chitonine polyplacophoran species but not to acanthochitonine Polyplacophora. Complete mitochondrial genome of Laevipilina antarctica.

Project description:BackgroundMitochondrial (mt) gene arrangement is highly variable among molluscs and especially among bivalves. Of the 30 complete molluscan mt-genomes published to date, only one is of a heterodont bivalve, although this is the most diverse taxon in terms of species numbers. We determined the complete sequence of the mitochondrial genomes of Acanthocardia tuberculata and Hiatella arctica, (Mollusca, Bivalvia, Heterodonta) and describe their gene contents and genome organisations to assess the variability of these features among the Bivalvia and their value for phylogenetic inference.ResultsThe size of the mt-genome in Acanthocardia tuberculata is 16.104 basepairs (bp), and in Hiatella arctica 18.244 bp. The Acanthocardia mt-genome contains 12 of the typical protein coding genes, lacking the Atpase subunit 8 (atp8) gene, as all published marine bivalves. In contrast, a complete atp8 gene is present in Hiatella arctica. In addition, we found a putative truncated atp8 gene when re-annotating the mt-genome of Venerupis philippinarum. Both mt-genomes reported here encode all genes on the same strand and have an additional trnM. In Acanthocardia several large non-coding regions are present. One of these contains 3.5 nearly identical copies of a 167 bp motive. In Hiatella, the 3' end of the NADH dehydrogenase subunit (nad)6 gene is duplicated together with the adjacent non-coding region. The gene arrangement of Hiatella is markedly different from all other known molluscan mt-genomes, that of Acanthocardia shows few identities with the Venerupis philippinarum. Phylogenetic analyses on amino acid and nucleotide levels robustly support the Heterodonta and the sister group relationship of Acanthocardia and Venerupis. Monophyletic Bivalvia are resolved only by a Bayesian inference of the nucleotide data set. In all other analyses the two unionid species, being to only ones with genes located on both strands, do not group with the remaining bivalves.ConclusionThe two mt-genomes reported here add to and underline the high variability of gene order and presence of duplications in bivalve and molluscan taxa. Some genomic traits like the loss of the atp8 gene or the encoding of all genes on the same strand are homoplastic among the Bivalvia. These characters, gene order, and the nucleotide sequence data show considerable potential of resolving phylogenetic patterns at lower taxonomic levels.

Project description:BackgroundComplete mitochondrial (mt) genomes have been used extensively to test hypotheses about microevolution and to study population structure, phylogeography, and phylogenetic relationships of Anura at various taxonomic levels. Large-scale mt genomic reorganizations have been observed among many fork-tongued frogs (family Dicroglossidae). The relationships among Dicroglossidae and validation of the genus Feirana are still problematic. Hence, we sequenced the complete mt genomes of Nanorana taihangnica (=F. taihangnica) and N. yunnanensis as well as partial mt genomes of six Quasipaa species (dicroglossid taxa), two Odorrana and two Amolops species (Ranidae), and one Rhacophorus species (Rhacophoridae) in order to identify unknown mt gene rearrangements, to investigate the validity of the genus Feirana, and to test the phylogenetic relationship of Dicroglossidae.ResultsIn the mt genome of N. taihangnica two trnM genes, two trnP genes and two control regions were found. In addition, the trnA, trnN, trnC, and trnQ genes were translocated from their typical positions. In the mt genome of N. yunnanensis, three control regions were found and eight genes (ND6, trnP, trnQ, trnA, trnN, trnC, trnY and trnS genes) in the L-stand were translocated from their typical position and grouped together. We also found intraspecific rearrangement of the mitochondrial genomes in N. taihangnica and Quasipaa boulengeri. In phylogenetic trees, the genus Feirana nested deeply within the clade of genus Nanorana, indicating that the genus Feirana may be a synonym to Nanorana. Ranidae as a sister clade to Dicroglossidae and the clade of (Ranidae + Dicroglossidae) as a sister clade to (Mantellidae + Rhacophoridae) were well supported in BI analysis but low bootstrap in ML analysis.ConclusionsWe found that the gene arrangements of N. taihangnica and N. yunnanensis differed from other published dicroglossid mt genomes. The gene arrangements in N. taihangnica and N. yunnanensis could be explained by the Tandem Duplication and Random Loss (TDRL) and the Dimer-Mitogenome and Non-Random Loss (DMNR) models, respectively. The invalidation of the genus Feirana is supported in this study.

Dataset Information

The complete mitochondrial genomes of six heterodont bivalves (Tellinoidea and Solenoidea): variable gene arrangements and phylogenetic implications.

Publications

The complete mitochondrial genomes of six heterodont bivalves (Tellinoidea and Solenoidea): variable gene arrangements and phylogenetic implications.

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