The Earliest Stages of Mitochondrial Adaptation to Low Oxygen Revealed in a Novel Rhizarian

Mitochondria exist on a functional and evolutionary continuum that includes anaerobic mitochondrion-related organelles (MROs), such as hydrogenosomes. Hydrogenosomes lack many classical mitochondrial features, including conspicuous cristae, mtDNA, the tricarboxylic acid (TCA) cycle, and ATP synthesis powered by an electron transport chain (ETC); instead, they produce ATP anaerobically, liberating H2 and CO2 gas in the process. However, our understanding of the evolutionary transformation from aerobic mitochondria to various MRO types remains incomplete. Here we describe a novel MRO from a cercomonad (Brevimastigomonas motovehiculus n. sp.; Rhizaria). We have sequenced its 30,608-bp mtDNA and characterized organelle function through a combination of transcriptomic, genomic, and cell biological approaches. B. motovehiculus MROs are metabolically versatile, retaining mitochondrial metabolic pathways, such as a TCA cycle and ETC-driven ATP synthesis, but also possessing hydrogenosomal-type pyruvate metabolism and substrate-level phosphorylation. Notably, the B. motovehiculus ETC is degenerate and appears to be losing cytochrome-based electron transport (complexes III and IV). Furthermore, the F1Fo ATP synthase (complex V) is unique, with the highly conserved Atpα subunit fragmented into four separate pieces. The B. motovehiculus MRO appears to be in the process of losing aerobic metabolic capacities. Our findings shed light on the transition between organelle types, specifically the early stages of mitochondrial adaptation to anaerobiosis. •Microaerobic B. motovehiculus mitochondria are metabolically versatile•A transitional organelle combines mitochondrial and hydrogenosomal attributes•Aerobic metabolism is degenerating, with loss and fragmentation of key genes•This work is a window into the evolutionary adaptation of mitochondria to low oxygen Gawryluk et al. report a complex transitional organelle that reveals key links between mitochondria and hydrogenosomes. Their investigation points to a general model of adaptation to life at low oxygen via loss and degeneration of critical aerobic genes, in concert with lateral gene transfer-mediated acquisition of anaerobic metabolism.