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Comparative analysis of the complete mitochondrial genomes in two limpets from Lottiidae (Gastropoda: Patellogastropoda): rare irregular gene rearrangement within Gastropoda.

ABSTRACT: To improve the systematics and taxonomy of Patellogastropoda within the evolution of gastropods, we determined the complete mitochondrial genome sequences of Lottia goshimai and Nipponacmea fuscoviridis in the family Lottiidae, which presented sizes of 18,192 bp and 18,720 bp, respectively. In addition to 37 common genes among metazoa, we observed duplication of the trnM gene in L. goshimai and the trnM and trnW genes in N. fuscoviridis. The highest A + T contents of the two species were found within protein-coding genes (59.95% and 54.55%), followed by rRNAs (56.50% and 52.44%) and tRNAs (56.42% and 52.41%). trnS1 and trnS2 could not form the canonical cloverleaf secondary structure due to the lack of a dihydrouracil arm in both species. The gene arrangements in all Patellogastropoda compared with those of ancestral gastropods showed different levels of gene rearrangement, including the shuffling, translocation and inversion of single genes or gene fragments. This kind of irregular rearrangement is particularly obvious in the Lottiidae family. The results of phylogenetic and gene rearrangement analyses showed that L. goshimai and Lottia digitalis clustered into one group, which in turn clustered with N. fuscoviridis in Patellogastropoda. This study demonstrates the significance of complete mitogenomes for phylogenetic analysis and enhances our understanding of the evolution of Patellogastropoda.

SUBMITTER: Feng JT

PROVIDER: S-EPMC7648102 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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.

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Comparative analysis of the complete mitochondrial genomes in two limpets from Lottiidae (Gastropoda: Patellogastropoda): rare irregular gene rearrangement within Gastropoda.

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