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The complete mitochondrial genome of Solemya velum (Mollusca: Bivalvia) and its relationships with conchifera.

ABSTRACT: BACKGROUND: Bivalve mitochondrial genomes exhibit a wide array of uncommon features, like extensive gene rearrangements, large sizes, and unusual ways of inheritance. Species pertaining to the order Solemyida (subclass Opponobranchia) show many peculiar evolutionary adaptations, f.i. extensive symbiosis with chemoautotrophic bacteria. Despite Opponobranchia are central in bivalve phylogeny, being considered the sister group of all Autobranchia, a complete mitochondrial genome has not been sequenced yet. RESULTS: In this paper, we characterized the complete mitochondrial genome of the Atlantic awning clam Solemya velum: A-T content, gene arrangement and other features are more similar to putative ancestral mollusks than to other bivalves. Two supranumerary open reading frames are present in a large, otherwise unassigned, region, while the origin of replication could be located in a region upstream to the cox3 gene. CONCLUSIONS: We show that S. velum mitogenome retains most of the ancestral conchiferan features, which is unusual among bivalve mollusks, and we discuss main peculiarities of this first example of an organellar genome coming from the subclass Opponobranchia. Mitochondrial genomes of Solemya (for bivalves) and Haliotis (for gastropods) seem to retain the original condition of mollusks, as most probably exemplified by Katharina.

SUBMITTER: Plazzi F

PROVIDER: S-EPMC3704766 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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The complete mitochondrial genome of Solemya velum (Mollusca: Bivalvia) and its relationships with conchifera.

Plazzi Federico F Ribani Anisa A Passamonti Marco M

BMC genomics 20130618

<h4>Background</h4>Bivalve mitochondrial genomes exhibit a wide array of uncommon features, like extensive gene rearrangements, large sizes, and unusual ways of inheritance. Species pertaining to the order Solemyida (subclass Opponobranchia) show many peculiar evolutionary adaptations, f.i. extensive symbiosis with chemoautotrophic bacteria. Despite Opponobranchia are central in bivalve phylogeny, being considered the sister group of all Autobranchia, a complete mitochondrial genome has not been ...[more]

PMID: 23777315

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Project description:BACKGROUND: Reconstructing the higher relationships of pulmonate gastropods has been difficult. The use of morphology is problematic due to high homoplasy. Molecular studies have suffered from low taxon sampling. Forty-eight complete mitochondrial genomes are available for gastropods, ten of which are pulmonates. Here are presented the new complete mitochondrial genomes of the ten following species of pulmonates: Salinator rhamphidia (Amphiboloidea); Auriculinella bidentata, Myosotella myosotis, Ovatella vulcani, and Pedipes pedipes (Ellobiidae); Peronia peronii (Onchidiidae); Siphonaria gigas (Siphonariidae); Succinea putris (Stylommatophora); Trimusculus reticulatus (Trimusculidae); and Rhopalocaulis grandidieri (Veronicellidae). Also, 94 new pulmonate-specific primers across the entire mitochondrial genome are provided, which were designed for amplifying entire mitochondrial genomes through short reactions and closing gaps after shotgun sequencing. RESULTS: The structural features of the 10 new mitochondrial genomes are provided. All genomes share similar gene orders. Phylogenetic analyses were performed including the 10 new genomes and 17 genomes from Genbank (outgroups, opisthobranchs, and other pulmonates). Bayesian Inference and Maximum Likelihood analyses, based on the concatenated amino-acid sequences of the 13 protein-coding genes, produced the same topology. The pulmonates are paraphyletic and basal to the opisthobranchs that are monophyletic at the tip of the tree. Siphonaria, traditionally regarded as a basal pulmonate, is nested within opisthobranchs. Pyramidella, traditionally regarded as a basal (non-euthyneuran) heterobranch, is nested within pulmonates. Several hypotheses are rejected, such as the Systellommatophora, Geophila, and Eupulmonata. The Ellobiidae is polyphyletic, but the false limpet Trimusculus reticulatus is closely related to some ellobiids. CONCLUSIONS: Despite recent efforts for increasing the taxon sampling in euthyneuran (opisthobranchs and pulmonates) molecular phylogenies, several of the deeper nodes are still uncertain, because of low support values as well as some incongruence between analyses based on complete mitochondrial genomes and those based on individual genes (18S, 28S, 16S, CO1). Additional complete genomes are needed for pulmonates (especially for Williamia, Otina, and Smeagol), as well as basal heterobranchs closely related to euthyneurans. Increasing the number of markers for gastropod (and more broadly mollusk) phylogenetics also is necessary in order to resolve some of the deeper nodes -although clearly not an easy task. Step by step, however, new relationships are being unveiled, such as the close relationships between the false limpet Trimusculus and ellobiids, the nesting of pyramidelloids within pulmonates, and the close relationships of Siphonaria to sacoglossan opisthobranchs. The additional genomes presented here show that some species share an identical mitochondrial gene order due to convergence.

Project description:BackgroundMitochondria contain small genomes that are physically separate from those of nuclei. Their comparison serves as a model system for understanding the processes of genome evolution. Although complete mitochondrial genome sequences have been reported for more than 600 animals, the taxonomic sampling is highly biased toward vertebrates and arthropods, leaving much of the diversity yet uncharacterized.ResultsThe mitochondrial genome of the bellybutton nautilus, Nautilus macromphalus, a cephalopod mollusk, is 16,258 nts in length and 59.5% A+T, both values that are typical of animal mitochondrial genomes. It contains the 37 genes that are almost universally found in animal mtDNAs, with 15 on one DNA strand and 22 on the other. The arrangement of these genes can be derived from that of the distantly related Katharina tunicata (Mollusca: Polyplacophora) by a switch in position of two large blocks of genes and transpositions of four tRNA genes. There is strong skew in the distribution of nucleotides between the two strands, and analysis of this yields insight into modes of transcription and replication. There is an unusual number of non-coding regions and their function, if any, is not known; however, several of these demark abrupt shifts in nucleotide skew, and there are several identical sequence elements at these junctions, suggesting that they may play roles in transcription and/or replication. One of the non-coding regions contains multiple repeats of a tRNA-like sequence. Some of the tRNA genes appear to overlap on the same strand, but this could be resolved if the polycistron were cleaved at the beginning of the downstream gene, followed by polyadenylation of the product of the upstream gene to form a fully paired structure.ConclusionNautilus macromphalus mtDNA contains an expected gene content that has experienced few rearrangements since the evolutionary split between cephalopods and polyplacophorans. It contains an unusual number of non-coding regions, especially considering that these otherwise often are generated by the same processes that produce gene rearrangements. The skew in nucleotide composition between the two strands is strong and associated with the direction of transcription in various parts of the genomes, but a comparison with K. tunicata implies that mutational bias during replication also plays a role. This appears to be yet another case where polyadenylation of mitochondrial tRNAs restores what would otherwise be an incomplete structure.

Project description:Despite the large number of animal complete mitochondrial genomes currently available in public databases, knowledge about mitochondrial genomics in invertebrates is uneven. This paper reports, for the first time, the complete mitochondrial genome of the grooved carpet shell, Ruditapes decussatus, also known as the European clam. Ruditapes decussatus is morphologically and ecologically similar to the Manila clam Ruditapes philippinarum, which has been recently introduced for aquaculture in the very same habitats of Ruditapes decussatus, and that is replacing the native species. Currently the production of the European clam is almost insignificant, nonetheless it is considered a high value product, and therefore it is an economically important species, especially in Portugal, Spain and Italy. In this work we: (i) assembled Ruditapes decussatus mitochondrial genome from RNA-Seq data, and validated it by Sanger sequencing; (ii) analyzed and characterized the Ruditapes decussatus mitochondrial genome, comparing its features with those of other venerid bivalves; (iii) assessed mitochondrial sequence polymorphism (SP) and copy number variation (CNV) of tandem repeats across 26 samples. Despite using high-throughput approaches we did not find evidence for the presence of two sex-linked mitochondrial genomes, typical of the doubly uniparental inheritance of mitochondria, a phenomenon known in ?100 bivalve species. According to our analyses, Ruditapes decussatus is more genetically similar to species of the Genus Paphia than to the congeneric Ruditapes philippinarum, a finding that bolsters the already-proposed need of a taxonomic revision. We also found a quite low genetic variability across the examined samples, with few SPs and little variability of the sequences flanking the control region (Largest Unassigned Regions (LURs). Strikingly, although we found low nucleotide variability along the entire mitochondrial genome, we observed high levels of length polymorphism in the LUR due to CNV of tandem repeats, and even a LUR length heteroplasmy in two samples. It is not clear if the lack of genetic variability in the mitochondrial genome of Ruditapes decussatus is a cause or an effect of the ongoing replacement of Ruditapes decussatus with the invasive Ruditapes philippinarum, and more analyses, especially on nuclear sequences, are required to assess this point.

Project description:BackgroundDoubly Uniparental Inheritance (DUI) represents the most outstanding exception to matrilinear inheritance of mitochondrial DNA (mtDNA), typical of Metazoa. In a few bivalve mollusks, two sex-linked mtDNAs (the so-called M and F) are inherited in a peculiar way: both daughters and sons receive their F from the mother, whereas sons inherit M from the father (males do not transmit F to their progeny). This realizes a double mechanism of transmission, in which M and F mtDNAs are inherited uniparentally. DUI systems represent a unique experimental model for testing the evolutionary mechanisms that apply to mitochondrial genomes and their transmission patterns as well as to mtDNA recombination.ResultsA new case of DUI is described in Musculista senhousia (Mollusca: Bivalvia: Mytilidae). Its heteroplasmy pattern is in line with standard DUI. Sequence variability analysis evidenced two main results: F haplotypes sequence variability is higher than that of M haplotypes, and F mitochondrial haplotypes experience a higher mutation rate in males' somatic tissues than in females' ones. Phylogenetic analysis revealed also that M. senhousia M and F haplotypes cluster separately from that of the other mytilids.ConclusionSequence variability analysis evidenced some unexpected traits. The inverted variability pattern (the F being more variable than M) was new and it challenges most of the rationales proposed to account for sex-linked mtDNA evolution. We tentatively related this to the history of the Northern Adriatic populations analyzed. Moreover, F sequences evidenced a higher mutation level in male's soma, this variability being produced de novo each generation. This suggests that mechanisms evolved to protect mtDNA in females (f.i. antioxidant gene complexes) might be under relaxed selection in males. Phylogenetic analysis of sex-linked haplotypes confirmed that they have switched their roles during the evolutionary history of mytilids, at variance to what has been observed in unionids. Consequently, reciprocal monophyly of M and F lineages got easily lost because of role-reversals and consequent losses of M lineages, as already observed in Mytilus.

Dataset Information

The complete mitochondrial genome of Solemya velum (Mollusca: Bivalvia) and its relationships with conchifera.

Publications

The complete mitochondrial genome of Solemya velum (Mollusca: Bivalvia) and its relationships with conchifera.

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