Genomics of Preaxostyla Flagellates Illuminates Evolutionary Transitions and the Path Towards Mitochondrial Loss

Until recently, mitochondria were considered essential organelles impossible to truly lose in a lineage. This view changed in 2016, with the report that the oxymonad Monocercomonoides exilis, was the first known eukaryote without any mitochondrion. Questions remain, however, about whether this extends to the entire lineage and how this transition took place. Oxymonadida are a group of gut endobionts of insects, reptiles, and mammals. They are housed in the Preaxostyla (Metamonada), a protistan group that also contains free-living flagellates of genera Trimastix and Paratrimastix. These latter two taxa harbor conspicuous mitochondrion-related organelles (MROs), while no mitochondria were reported for any oxymonad. Here we report genomic data sets of two Preaxostyla representatives, the free-living Paratrimastix pyriformis and the oxymonad Blattamonas nauphoetae. We note that P. pyriformis possesses a set of unique or ancestral features among metamonads or eukaryotes, e.g., p-cresol synthesis, NAD+ synthesis, selenium volatilization, or mercury methylation, demonstrating the biochemical versatility of this protist lineage. We performed thorough comparisons among all available genomic and transcriptomic data of Preaxostyla to corroborate both the absence of MRO in Oxymonadida and the nature of MROs present in other Preaxostyla and to decipher the evolutionary transition towards amitochondriality and endobiosis. Our results provide insights into the metabolic and endomembrane evolution, but most strikingly the data confirm the complete loss of mitochondria and every protein that has ever participated in the mitochondrion function for all three oxymonad species (M. exilis, B. nauphoetae, and Streblomastix strix) extending the amitochondriate status to the whole Oxymonadida.