Abstract
BackgroundA novel feature for animal mitochondrial genomes has been recently established: i.e., the presence of additional, lineage-specific, mtDNA-encoded proteins with functional significance. This feature has been observed in freshwater mussels with doubly uniparental inheritance of mtDNA (DUI). The latter unique system of mtDNA transmission, which also exists in some marine mussels and marine clams, is characterized by one mt genome inherited from the female parent (F mtDNA) and one mt genome inherited from the male parent (M mtDNA). In freshwater mussels, the novel mtDNA-encoded proteins have been shown to be mt genome-specific (i.e., one novel protein for F genomes and one novel protein for M genomes). It has been hypothesized that these novel, F- and M-specific, mtDNA-encoded proteins (and/or other F- and/or M-specific mtDNA sequences) could be responsible for the different modes of mtDNA transmission in bivalves but this remains to be demonstrated.Methodology/Principal FindingsWe investigated all complete (or nearly complete) female- and male-transmitted marine mussel mtDNAs previously sequenced for the presence of ORFs that could have functional importance in these bivalves. Our results confirm the presence of a novel F genome-specific mt ORF, of significant length (>100aa) and located in the control region, that most likely has functional significance in marine mussels. The identification of this ORF in five Mytilus species suggests that it has been maintained in the mytilid lineage (subfamily Mytilinae) for ∼13 million years. Furthermore, this ORF likely has a homologue in the F mt genome of Musculista senhousia, a DUI-containing mytilid species in the subfamily Crenellinae. We present evidence supporting the functionality of this F-specific ORF at the transcriptional, amino acid and nucleotide levels.Conclusions/SignificanceOur results offer support for the hypothesis that “novel F genome-specific mitochondrial genes” are involved in key biological functions in bivalve species with DUI.
Highlights
Apart from the nucleus, mitochondria are the only known organelles with their own DNA in animal cells
To assess whether F and M mitochondrial control regions (CR) could possess open reading frames (ORFs) that could have functional importance in Mytilus bivalves, we first investigated complete mitochondrial DNA (mtDNA) previously sequenced for the Mytilus edulis species complex (i.e., M. edulis, M. galloprovincialis and M. trossulus of the subfamily Mytilinae)
Assessing homology using a combination of sequence and position similarity, M-type ORFs of 94aa and 112aa were found in M. edulis VD1, ORFs of 21 and 42aa were found in M. galloprovincialis and ORFs of 73aa and 74aa were found in M. trossulus VD1 (Tables 1 and 2)
Summary
Apart from the nucleus, mitochondria are the only known organelles with their own DNA in animal cells. Comparative mitochondrial genomics has revealed that animal mtDNAs are very conserved in terms of gene content [4]. These small circular and typically intron-less molecules encode 2 ribosomal RNAs, 22 transfer RNAs and 13 protein subunits of the mitochondrial respiratory chain complexes and ATP synthase. A novel feature for animal mitochondrial genomes has been recently established: i.e., the presence of additional, lineage-specific, mtDNA-encoded proteins with functional significance. This feature has been observed in freshwater mussels with doubly uniparental inheritance of mtDNA (DUI). It has been hypothesized that these novel, F- and M-specific, mtDNA-encoded proteins (and/or other Fand/or M-specific mtDNA sequences) could be responsible for the different modes of mtDNA transmission in bivalves but this remains to be demonstrated
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