Evolution of pathogenic and nonpathogenic yeasts mitochondrial genomes inferred by supertrees and supermatrices with divergence estimates based on relaxed molecular clocks

The evolution of mitochondrial genomes is essential for the adaptation of yeasts to the variation of environmental levels of oxygen. AlthoughSaccharomyces cerevisiaemitochondrial DNA lacks all complex I genes, respiration is possible because alternative NADH dehydrogenases are encoded byNDE1andNDI1nuclear genes. The proposed whole genome duplication (WGD) in the yeast ancestor at 150-100 million years ago caused nuclear gene duplications and secondary losses, although its relation to the loss of complex I mitocondrial is unknown. Here we present phylogenomic supertrees and supermatrix tree of 46 mitochondrial genomes showing that the loss of complex I predates WGD and occurred independently in theS. cerevisiaegroup and the fission yeastSchizosaccharomyces pombe. We also show that the branching patterns do not differ dramatically in supertrees and supermatrix phylogenies. Our inferences indicated 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 theSaccharomyceslineage might have lost the complex I during hypoxic periods near Perminian-Triassic or Triassic-Jurassic mass extinction events, while theSchizosaccharomyceslineage possibly lost the complex I during hypoxic environment periods during Middle Cambrian until Lower Devonian. The loss of mitochondrial complex I during low oxygen might not affect yeast metabolism due to fermentative switch. The return to increased oxygen periods might have favored adaptations to aerobic metabolism. Additionally, we also showed thatNDE1andNDI1phylogenies indicate evolutionary convergence in yeasts where mitochondrial complex I is absent.