Can’t be male without complex I? Alteration in cellular metabolism involved in cytoplasmic male sterility in snail Physa acuta

Cytoplasmic male sterility (CMS) is a well-known example of mitonuclear genetic conflict over sex determination in hermaphrodite plants, where mitochondrial genes maternally inherited sterilize the male function while biparental inherited nuclear genes restore it. CMS has been recently discovered in animals, in the freshwater snail Physa acuta . In this species, CMS is associated with two extremely divergent mitogenomes D and K compared to the classical mitogenome N. D individuals are male-steriles, while male fertility is restored in K individuals. We hypothesized that the extreme divergence of mitogenomes associated with CMS can impact mitochondrial aerobic metabolism, a necessary process in eukaryotic organisms by which energy is transduced from food to ATP. We show that CMS is associated with an alteration of co-encoded complex I in D male-sterile individuals, although partly compensated by the nuclear-encoded complex II. K restored hermaphrodites have an unaffected complex I respiration, but exhibit lower mitochondrial efficiency and higher anaerobic contribution to cellular metabolism, highlighting an energy cost of bearing CMS and restorer genes, which likely underlie the reduced growth of K mitotype. How complex I alteration induces male-sterility remains to be determined, but could be linked to oxidative stress or a defect in ATP-synthesis rate.