Impact of ancient oxygen levels on mitochondrial genome evolution inferred by supertrees, supermatrices, and relaxed molecular clocks
Evolution of mitochondrial genomes is essential for the adaptation of yeasts to changes in environmental oxygen levels. Although Saccharomyces cerevisiae mitochondrial DNA lacks all complex I genes, respiration is possible because alternative NADH dehydrogenases are encoded by NDE1 and NDI1 nuclear genes. The apparent whole genome duplication (WGD) in the yeast ancestor 100-150 million years ago caused nuclear gene duplications and secondary losses, although its relation to the loss of mitochondrial complex I is unknown. We produced phylogenomic supertrees and a supermatrix tree of 46 mitochondrial genomes, showing that the loss of complex I predates WGD and occurred independently in the S. cerevisiae group and the fission yeast Schizosaccharomyces pombe. The branching patterns did not differ substantially in supertrees and supermatrix phylogenies. We found consistent relations between conserved mitochondrial chromosomal gene order (synteny) in closely related yeasts. Correlation of mitochondrial molecular clock estimates and atmospheric oxygen variation in the Phanerozoic suggests that the Saccharomyces lineage might have lost complex I during hypoxic periods near Permian-Triassic or Triassic-Jurassic mass extinction events, while the Schizosaccharomyces lineage possibly lost complex I during hypoxic environment periods during the Middle Cambrian until the Lower Devonian. The loss of mitochondrial complex I, as a result of low oxygen levels, might not affect yeast metabolism due to a fermentative switch. The return to increased oxygen periods could have favored adaptations to aerobic metabolism. Additionally, we also show that NDE1 and NDI1 phylogenies indicate evolutionary convergence in yeasts in which mitochondrial complex I is absent.