Multiple invertebrates possess enzymes enabling de novo biosynthesis of essential omega-3 fatty acids.

Ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota are widespread in marine and terrestrial habitats, playing a major role in the global nitrogen cycle. However, their evolutionary history remains unexplored, which limits our understanding of their adaptation mechanisms. Here, our comprehensive phylogenomic tree of Thaumarchaeota supports three sequential events: origin of AOA from terrestrial non-AOA ancestors, colonization of the shallow ocean, and expansion to the deep ocean. Careful molecular dating suggests that these events coincided with the Great Oxygenation Event around 2300 million years ago (Mya), and oxygenation of the shallow and deep ocean around 800 and 635–560 Mya, respectively. The first transition was likely enabled by the gain of an aerobic pathway for energy production by ammonia oxidation and biosynthetic pathways for cobalamin and biotin that act as cofactors in aerobic metabolism. The first transition was also accompanied by the loss of dissimilatory nitrate and sulfate reduction, loss of oxygen-sensitive pyruvate oxidoreductase, which reduces pyruvate to acetyl-CoA, and loss of the Wood–Ljungdahl pathway for anaerobic carbon fixation. The second transition involved gain of a K⁺ transporter and of the biosynthetic pathway for ectoine, which may function as an osmoprotectant. The third transition was accompanied by the loss of the uvr system for repairing ultraviolet light-induced DNA lesions. We conclude that oxygen availability drove the terrestrial origin of AOA and their expansion to the photic and dark oceans, and that the stressors encountered during these events were partially overcome by gene acquisitions from Euryarchaeota and Bacteria, among other sources.

Mitochondria play a fundamental role in cellular metabolism, being responsible for most of the energy production of the cell in the oxidative phosphorylation (OXPHOS) pathway. Mitochondrial DNA (mtDNA) encodes for key components of this process, but its direct role in adaptation remains far from understood. Hares (Lepus spp.) are privileged models to study the impact of natural selection on mitogenomic evolution because 1) species are adapted to contrasting environments, including arctic, with different metabolic pressures, and 2) mtDNA introgression from arctic into temperate species is widespread. Here, we analyzed the sequences of 11 complete mitogenomes (ten newly obtained) of hares of temperate and arctic origins (including two of arctic origin introgressed into temperate species). The analysis of patterns of codon substitutions along the reconstructed phylogeny showed evidence for positive selection in several codons in genes of the OXPHOS complexes, most notably affecting the arctic lineage. However, using theoretical models, no predictable effect of these differences was found on the structure and physicochemical properties of the encoded proteins, suggesting that the focus of selection may lie on complex interactions with nuclear encoded peptides. Also, a cloverleaf structure was detected in the control region only from the arctic mtDNA lineage, which may influence mtDNA replication and transcription. These results suggest that adaptation impacted the evolution of hare mtDNA and may have influenced the occurrence and consequences of the many reported cases of massive mtDNA introgression. However, the origin of adaptation remains elusive.

Mitochondrial genomes are known to have a strong strand-specific compositional bias that is more pronounced at fourfold redundant sites of mtDNA protein-coding genes. This observation suggests that strand asymmetries, to a large extent, are caused by mutational asymmetric mechanisms. In vertebrate mitogenomes, replication and not transcription seems to play a major role in shaping compositional bias. Hence, one can better understand how mtDNA is replicated – a debated issue – through a detailed picture of mitochondrial genome evolution. Here, we analyzed the compositional bias (AT and GC skews) in protein-coding genes of almost 2,500 complete vertebrate mitogenomes. We were able to identify three fish mitogenomes with inverted AT/GC skew coupled with an inversion of the Control Region. These findings suggest that the vertebrate mitochondrial replication mechanism is asymmetric and may invert its polarity, with the leading-strand becoming the lagging-strand and vice-versa, without compromising mtDNA maintenance and expression. The inversion of the strand-specific compositional bias through the inversion of the Control Region is in agreement with the strand-displacement model but it is also compatible with the RITOLS model of mtDNA replication.