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.

Chromosome-level genome assembly of the disco clam,Ctenoides ales, a first for the bivalve order Limida

“…Mollusks exhibit some of the most variable genomic architecture, molecular functions, and patterns of inheritance for mitochondria in metazoans (reviewed in Ghiselli et al 2021). Pteriomorphian bivalves are known for dynamic mitochondrial (mt) genome evolution, with Arcidae having repeatedly evolved some of the largest bilaterian mt genomes (Kong et al 2020), and Pectinidae with frequent gene order rearrangements (Malkócs et al 2022) and species with exceptionally large mt genomes (e.g., La Roche et al 1990). Currently, around 300 complete or nearly complete mitochondrial genomes are publicly available on NCBI GenBank, none of which are from Limida.…”

“…The only typical metazoan protein coding gene not annotated was atp8, which is commonly absent in bivalve mitogenomes (Serb and Lydeard 2003). However, recent analyses support the presence of atp8 sequences in Pectinidae (Malkócs et al 2022) and Mytilidae (Zhao et al 2022).…”

The Complete Mitochondrial Genomes of Two Rock Scallops (Bivalvia: Spondylidae) Indicate Extensive Gene Rearrangements and Adaptive Evolution Compared with Pectinidae

“…Even though the current topology is highly supported, it is inconsistent with a previous phylogeny in which Aequipectinini was placed in the basal clade within Pectinidae [ 36 ]. Malkócs et al [ 24 ] concluded that different molecular markers could result in different topologies of Pectinidae, as indicated in other mollusk groups [ 25 , 37 ]. When the mitochondrial PCGs were used for phylogenetic analysis, Aequipectini always formed within Pectininae and in accordance with our result, while the topology derived from mitochondrial rRNA and nuclear H3 genes supported that of Puslednik and Serb [ 36 ].…”

“…Compared with other metazoans, mollusks are more prone to gene rearrangements [ 21 , 22 , 23 ]. In pectinids, mitochondrial gene rearrangements involve protein-coding genes (PCGs), ribosomal RNA (rRNA) genes, and transfer RNA (tRNA) genes, and considerable gene order changes could be detected even at the level of tribes [ 24 ]. However, the mitochondrial gene rearrangements within Pectinoidea other than Pectinidae have never been detected before.…”

MitoHiFi: a python pipeline for mitochondrial genome assembly from PacBio High Fidelity reads

“…The default parameter for coverage is set to 50% (i.e., at least 50% of the sequence of the contig has to be present in the BLAST match with the closely-related species mitochondrial genome), but this may be raised as high as 90% where the species being analysed is part of a richly-sampled group with highly constrained genome content and structure, such as Vertebrata. However, for other taxa such as Hymenoptera and Mollusca, the 50% match length cutoff is required (and indeed may be too strict) because these clades have mitochondrial genomes with highly variable gene orders [24] and a diversity of repeat lengths and copy numbers. For taxa with known variability, it is recommended that the pipeline is run using multiple different references (using the findMitoReference.py -n flag) and exploring different match length proportions.…”