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.

Figure 1

Genomic map and annotation of S. velum complete mitochondrial genome. Genes located on the external side of the map are on “ + ” strand (i.e. that encoding cox1), whereas genes on the internal side are on “-” strand. URs > 100 bp are shown and they were arbitrarily set on “ + ” strand. UNs, number of unassigned nucleotides after the gene: if negative, overlapping nucleotides with the following gene; PCG, Protein Coding Gene.

Figure 2

Compositional patterns of S. velum and other mollusks mitochondrial genomes. A-T content, A-T skew, and G-C skew are computed for each single gene and for many genomic regions following the legend below the chart.

Figure 3

A-C and G-T content along the mitochondrial genome of S. velum. A-C (pale blue) and G-T (dark red) contents are computed on a sliding window of size 151 bp. A linear sketch of the complete genome as annotated in Figure 1 is depicted above the plot: blue, PCGs; green, tRNAs; brown, rRNAs; gray, URs >100 bp; genes on the “ + ” strand are above the black line and genes on the “-” strand are below it.

Figure 4

Location of the origin of replication of the H strand. A (green), C (blue), G (black), and T (red) content at four-fold degenerate codons of PGCs are shown. Percent contents of each PCG are plotted at the midpoint of the ORF using the first nucleotide of cox3 ORF as the starting point. We also included ORF117 in this analysis (see text for further details). Equations are as follows. %A, y = 0.0017 × + 39.88, r² = 0.64, p < 0.005;%C, y = 0.0001 × 15.07, r² = 0.01, p = 0.71;%G, y = − 0.0009 × 14.09, r² = 0.30, p < 0.05;%T, y = − 0.0009 × 30.96, r² = 0.39, p < 0.05.

Figure 5

UR secondary structures. Putative secondary structures of largest URs of S. velum mitochondrial genome were inferred by software Mfold. The Gibbs energy (dG) is shown at the bottom of each structure. a, UR7; b, UR8.

Figure 6

Maximum likelihood (ML) tree. The tree shown is the consensus tree of 200 standard bootstrap replicates and the bootstrap proportion (BP) is shown for each node. Bivalves are shown in red; the asterisk indicates Solemya velum.

Figure 7

Gene rearrangements. Reconstruction of relationships among gene arrangements of Katharina tunicata/Haliotis rubra/Haliotis tuberculata, Solemya velum, C. nitidulum, Caenogastropoda, N. macromphalus, and S. officinalis is shown, after the exclusion of tRNAs. Genes involved in the rearrangements are shaded in gray. If a minus sign (“-”) is present, the gene is encoded on the “-” strand, otherwise it is encoded on the “ + ” strand. The asterisk is to signal that D. gregarium is an exception to the displayed common gene arrangement of Caenogastropoda; square brackets refer to a possible gene arrangement ancestral to N. macromphalus (subclass Nautiloida) and S. officinalis.