Co-expressed mitochondrial genomes: recently masculinized, recombinant mitochondrial genome is co-expressed with the female – transmitted mtDNA genome in a male Mytilus trossulus mussel from the Baltic Sea

Abstract

BackgroundFew exceptions have been described from strict maternal inheritance of mitochondrial DNA in animals, including sea mussels (Mytilidae), clams (Donacidae, Veneridae and Solenidae) and freshwater mussels (Unionoidae) order. In these bivalves mitochondria and their DNA are transferred through two separate routes. The females inherit only the maternal mitochondrial DNA whereas the males inherit maternal as well as paternal mitochondrial DNA, which is usually present only in gonads and sperm. The mechanism controlling this phenomenon is unclear but leads to the existence of two separate mitochondrial DNA lineages in a single species. The lineages are usually well differentiated: up to 20-50% divergence in nucleotide sequence. Occasionally, a maternal mitochondrial DNA can invade the paternal transmission route, eventually replacing the diverged M-type and lowering the divergence. Such role reversal (masculinization) event has happened recently in the Mytilus population of the Baltic Sea which consists of M. edulis × M. trossulus hybrids, but the functional status of the resulting mitochondrial genome was unknown.ResultsIn this paper we sequenced transcripts from one specimen that was identified as male carrying both the female mitochondrial genome and a recently masculinized mitochondrial genome. Additionally, the analysis of the control region has showed that the recently masculinized, recombinant genome, not only has an M-type control region and all coding regions derived from the F-type, but also is transcriptionally active along side the maternally inherited F-type genome. In the comparative analysis, the two genomes exhibit different substitution patterns, typical for the M vs. F genome comparisons. The genetic distances and ratios of non-synonymous substitutions also suggest that one of the genomes is transitioning from the maternal to the paternal inheritance mode, consistent with its recent masculinization.ConclusionWe have shown, for the first time, that the recently masculinized mitochondrial genome is active and that it accumulates excess of non-synonymous substitutions across its coding sequence. This suggests, that, under certain cytonuclear incompatibility conditions, masculinization may serve to restore the endangered functionality of the paternally inherited genome. This is also another example of a mitochondrial genome in which the recombination in the control region predated its transition from paternal to maternal transmission route.

Mitogenomics of recombinant mitochondrial genomes of Baltic Sea Mytilus mussels

“…The recent advances in transcriptomics (Chatzoglou et al 2013 ) allow more precise annotation of some protein-coding genes within this diverse data set. Our proposal to extend the nad5 gene is consistent with the notion that polycistronic transcript consisting of nad4l , nad5 , and nad6 is expressed in Mytilus (Chatzoglou et al 2013 ; Sańko and Burzyński 2014 ). The fragment we propose to include as coding is present within the transcript.…”

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

“…To verify the presence of DUI the following procedure was used for LCP1 sample. RNA was extracted and sequenced by RNA-Seq (Illumina MiSeq platform, Macrogen, South Korea) to verify the presence of two sets of transcripts, as described previously ( Sańko & Burzyński, 2014 ; Lubośny et al, 2017 ; Soroka et al, 2018 ). The resulting raw reads are available in SRA database under accession number SRR7504388 .…”

Next-generation sequencing of Dreissena polymorpha transcriptome sheds light on its mitochondrial DNA

“…This may be due to the bicistronic nature of its transcript and the fact that library construction involves priming of the first strand cDNA synthesis from the oligo-dT-based primer which may contribute to the under-representation of 3 0 ends of transcripts in the library. Bicistronic transcripts have been observed previously in other bivalves (Chatzoglou et al, 2013;Sańko & Burzyński, 2014). The phylogenetic relationships within Bivalvia are a matter of ongoing debate.…”

“…Fresh animals were transported to the laboratory, sexed by microscopic examination of gonadal tissues. Both RNA and DNA were extracted from mantle/gonadal tissue of the same male individual using established protocols (Sańko & Burzyński, 2014). The total RNA sample was sent to Macrogen (South Korea).…”