Mitogenomics ofPerumytilus purpuratus(Bivalvia: Mytilidae) and its implications for doubly uniparental inheritance of mitochondria

Abstract

Animal mitochondria are usually inherited through the maternal lineage. The exceptional system allowing fathers to transmit their mitochondria to the offspring exists in some bivalves. Its taxonomic spread is poorly understood and new mitogenomic data are needed to fill the gap. Here, we present for the first time the two divergent mitogenomes from Chilean mussel Perumytilus purpuratus. The existence of these sex-specific mitogenomes confirms that this species has the doubly uniparental inheritance (DUI) of mitochondria. The genetic distance between the two mitochondrial lineages in P. purpuratus is not only much bigger than in the Mytilus edulis species complex but also greater than the distance observed in Musculista senhousia, the only other DUI-positive member of the Mytilidae family for which both complete mitochondrial genomes were published to date. One additional, long ORF (open reading frame) is present exclusively in the maternal mitogenome of P. purpuratus. This ORF evolves under purifying selection, and will likely be a target for future DUI research.

Mitochondrial genomic analyses provide new insights into the “missing” atp8 and adaptive evolution of Mytilidae

“…4 Phylogenetic relationships of Mytilidae species based on 12 protein-coding genes using Bayesian inference and maximum likelihood methods. * Note: The sequence (KM655841.1) may from Mytilaster solisianus rather than "Perna Perna" [3] Mytilisepta + Perumytilus + Semimytilus, which was similar to the results of nuclear genes18S and 28S [75]. However, the placement of Geukensia was inconsistent.…”

“…The typical mitochondrial genome of animals is a small (16 kb) circular molecule, which includes 13 OXPHOS-related genes, 22 transfer RNA (tRNA) genes and 2 ribosomal RNA (rRNA) genes [1,2], and it usually follows a strictly maternal inheritance. In bivalves, some species of Mytilidae [2,3], Donacidae [4] and etc. showed a unique Doubly Uniparental Inheritance (DUI) model.…”

An Unusual Evolutionary Strategy: The Origins, Genetic Repertoire, and Implications of Doubly Uniparental Inheritance of Mitochondrial DNA in Bivalves

“…For example, the often duplicated tRNAMet gene in Mytilidae species(Hoffmann et al 1992;Mizi et al, 2005;Passamonti et al 2011;Śmietanka et al 2018) among other cases of tRNA gene duplications in specific lineages (see for examplesGuerra et al 2017 andLubośny et al 2020). More remarkable is the duplicated cox2 gene in the F mitogenome of the clam Ruditapes philippinarum or in the M genome of the mytilid Musculista senhousia, although their roles are still unknown(Passamonti et al, 2011;Ghiselli et al 2013;Breton et al 2014).…”

No evidence of DUI in the Mediterranean alien species Brachidontes pharaonis (P. Fisher, 1870) despite mitochondrial heteroplasmy

“…This hints that the taxonomy of M. solisianus may require reconsideration. Nevertheless, the phylogenetic distance between the two B. pharaonis mitogenomes is similar to the intraspecies distance between F-type mitogenomes form north and south populations of the Chilean mussels Perumytilus purpuratus which were separated from each other in Pleistocene 30 – 32 . It is also greater than the distance between several interspecies pairs of mitogenomes: Mytilus edulis and M. galloprovincialis , Bathmodiolus marisindicus and B. septemdierum, as well as all available mitogenomes form genus Gigantidas.…”