Metabolic remodelling associated with mtDNA: insights into the adaptive value of doubly uniparental inheritance of mitochondria

Abstract

Mitochondria produce energy through oxidative phosphorylation (OXPHOS), which depends on the expression of both nuclear and mitochondrial DNA (mtDNA). In metazoans, a striking exception from strictly maternal inheritance of mitochondria is doubly uniparental inheritance (DUI). This unique system involves the maintenance of two highly divergent mtDNAs (F-and M-type, 8-40% of nucleotide divergence) associated with gametes, and occasionally coexisting in somatic tissues. To address whether metabolic differences underlie this condition, we characterized the OXPHOS activity of oocytes, spermatozoa, and gills of different species through respirometry. DUI species express different gender-linked mitochondrial phenotypes in gametes and partly in somatic tissues. The M-phenotype is specific to sperm and entails (i) low coupled/uncoupled respiration rates, (ii) a limitation by the phosphorylation system, and (iii) a null excess capacity of the final oxidases, supporting a strong control over the upstream complexes. To our knowledge, this is the first example of a phenotype resulting from direct selection on sperm mitochondria. This metabolic remodelling suggests an adaptive value of mtDNA variations and we propose that bearing sex-linked mitochondria could assure the energetic requirements of different gametes, potentially linking male-energetic adaptation, mitotype preservation and inheritance, as well as resistance to both heteroplasmy and ageing.

Unorthodox features in two venerid bivalves with doubly uniparental inheritance of mitochondria

“…Hence the way (or ways) in which males of bivalves with DUI can tolerate heteroplasmy characterized by such high variability remains an important unanswered question (e.g. see Bettinazzi et al 66 ). Our results also highlighted an extremely unusual feature of the M genomes of S. plana and L. balthica compared to their female-transmitted counterparts.…”

An Unusual Evolutionary Strategy: The Origins, Genetic Repertoire, and Implications of Doubly Uniparental Inheritance of Mitochondrial DNA in Bivalves

“…Conversely, for the DUI species Arctica islandica and M. edulis, they express convergent OXPHOS remodelling in sperm mitochondria. M-type mitochondria in sperm and male somatic heteroplasmic tissues show functional divergence in OXPHOS activity and organization compared to F-type mitochondria present in eggs and female somatic tissues, involving a strong limitation of the electron transport system (ETS) by the phosphorylation system and a minimal spare capacity at cytochrome c oxidase (Bettinazzi et al 2019). Congruently, a lower activity of cytochrome c oxidase (CCO) was also detected for M. edulis M-type sperm, in comparison with the F-type "masculinized" ones (Breton et al 2009b).…”

“…The existence of a specific DUI mitochondrial remodelling, together with the fact that DUI sperm energetic strategy tightly relies on mitochondrial respiration, support the expectation that the selective forces driving the evolution of sperm mitochondria in absence of SMI might affect mt encoded components of respiratory complexes, thus foster change in the OXPHOS mechanisms and organization (Breton et al 2007;Breton et al 2009b). The overdescribed architecture provides unusual respiratory control at the terminus of the respiratory chain, high sensitivity to oxygen content in the medium, a potential high ROS flux and, interestingly, the capacity to preserve high membrane potential in sperm mitochondria (Bettinazzi et al 2019). Accumulating evidence supports this idea that DUI male mitochondria possess the ability to preserve a high mitochondrial membrane potential (Δψm).…”

The deteriorating soma and the indispensable germline: gamete senescence and offspring fitness

“…Both sexes usually only contain F-type mitochondria in their somatic tissues, but their gametes contain only the sex-specific form of mitochondria (i.e. M-type in sperm and F-type in oocytes) [147]. This means that M-type mitochondria must be passed on by fathers to the germline of their sons.…”

“…It is thus an unresolved question as to how these DUI species manage to prevent oxidatively damaged mitochondria from being passed to offspring. The two types of mitochondria in gametes have recently been shown to differ in their functioning, but in ways that would actually appear to increase the risk of oxidative damage to M-type mitochondria in the sperm [147]; this is so even in Arctica islandica, which can live to over 500 years and is thus the longest-lived non-colonial metazoan [150]. Whether the existence of DUI refutes the concept of the 'division of labour' as a means to prevent the inheritance of an aged phenotype is unresolved [149,151].…”