Metabolic consequences of naturally occurring mitochondrial heteroplasmy in bivalves

Oxidative phosphorylation, the cornerstone of mitochondrial energy production, is a tightly regulated process that relies on the strict interaction between mitochondrial and nuclear genomes. This intricate relationship requires the two genomes to coevolve to maintain mitochondrial function. However, when multiple mitochondrial variants coexist within an individual, a phenomenon known as heteroplasmy, this delicate balance can be disrupted, leading to bioenergetic inefficiencies and diseases. Interestingly, heteroplasmy naturally occurs in over a hundred species of bivalve molluscs, where paternal mitochondrial DNA is, in theory, exclusively inherited by male offspring and segregates in male gametes. Here, we leveraged this unique natural system to investigate the sex-specific distribution and translation pattern of somatic heteroplasmy, along with its impact on cellular bioenergetics in the bivalve species Mytilus edulis and Ruditapes philippinarum. By examining the relationship between heteroplasmy levels, haplotype expression and key enzymes involved in energy production, we uncovered unexpected findings. Contrary to predictions, somatic heteroplasmy was prevalent in both sexes and across both species. While heteroplasmy did not significantly affect overall bioenergetics, females of M. edulis showed notable exceptions in their gills. Possible compensatory mechanisms and species- or sex-specific adaptation to heteroplasmy are discussed.