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Mitogenomics of recombinant mitochondrial genomes of Baltic Sea Mytilus mussels.

ABSTRACT: Recombination in the control region (CR) of Mytilus mitochondrial DNA (mtDNA) was originally reported based on the relatively short, sequenced fragments of mitochondrial genomes. Recombination outside the CR has been reported recently with the suggestion that such processes are common in Mytilus. We have fully sequenced a set of 11 different mitochondrial haplotypes representing the high diversity of paternally inherited mitochondrial genomes of Baltic Sea Mytilus mussels, including the haplotype close to the native Mytilus trossulus mitochondrial genome, which was thought to have been entirely eliminated from this population. Phylogenetic and comparative analysis showed that the recombination is limited to the vicinity of the CR in all sequenced genomes. Coding sequence comparison indicated that all paternally inherited genomes showed increased accumulation of nonsynonymous substitutions, including the genomes which switched their transmission route very recently. The acquisition of certain CR sequences through recombination with highly divergent paternally inherited genomes seems to precede and favor the switch, but it is not a prerequisite for this process. Interspecies hybridization in the Baltic Sea during the recent 10,000 years created conditions for both structural and evolutionary mitochondrial instability which resulted in the observed variation and dynamics of mtDNA in Baltic Sea Mytilus mussels. In conclusion, the data shows that the effects of mitochondrial recombination are limited to the CR of few phylogenetic lineages.

SUBMITTER: Zbawicka M

PROVIDER: S-EPMC4236608 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.

Project description:Two blue mussel lineages of Pliocene origin, Mytilus edulis (ME) and M. trossulus (MT), co-occur and hybridize in several regions on the shores of the North Atlantic. The two species were distinguished from each other by molecular methods in the 1980s, and a large amount of comparative data on them has been accumulated since that time. However, while ME and MT are now routinely distinguished by various genetic markers, they tend to be overlooked in ecological studies since morphological characters for taxonomic identification have been lacking, and no consistent habitat differences between lineages have been reported. Surveying a recently discovered area of ME and MT co-occurrence in the White Sea and employing a set of allozyme markers for identification, we address the issue whether ME and MT are true biological species with distinct ecological characteristics or just virtual genetic entities with no matching morphological and ecological identities. We find that: (1) in the White Sea, the occurrence of MT is largely concentrated in harbors, in line with observations from other subarctic regions of Europe; (2) mixed populations of ME and MT are always dominated by purebred individuals, animals classified as hybrids constituting only ca. 18%; (3) in terms of shell morphology, 80% of MT bear a distinct uninterrupted dark prismatic strip under the ligament while 97% of ME lack this character; (4) at sites of sympatry MT is more common on algal substrates while ME mostly lives directly on the bottom. This segregation by the substrate may contribute to maintaining reproductive isolation and decreasing competition between taxa. We conclude that while ME and MT are not fully reproductively isolated, they do represent clearly distinguishable biological, ecological and morphological entities in the White Sea. It remains to be documented whether the observed morphological and ecological differences are of a local character, or whether they have simply been overlooked in other contact zones.

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Mitogenomics of recombinant mitochondrial genomes of Baltic Sea Mytilus mussels.

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