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Background Leontynka is a non-photosynthetic lineage of the order Chlamydomonadales (Chlorophyta). Although many Chlamydomonadales members encode components of the anaerobic energy metabolism, studies focused on Chlamydomonadales algae thriving in hypoxia and not prospering in oxic conditions are missing. Using a combination of experimental approaches, comparative genomics, and advanced in silico protein localization analyses, we employed Leontynka as a model to investigate the evolution of anaerobiosis in Chlamydomonadales. Results Leontynka spp. accumulate a wide range of storage forms, enabling them to cope with nutritional stresses. Their mitochondria contain well-developed cristae mediating a conventional aerobic energy metabolism. Moreover, colocalization of a Raman signal for cytochromes with the position of mitochondria in the cell indicates that oxidative phosphorylation is an important route of energy metabolism in the alga. Interestingly, Leontynka spp. concentrate enzymes potentially involved in oxygen-independent ATP synthesis within the plastid, which lost the ability to produce ATP using proton gradient generated by membrane complexes that exploit redox reactions. We analyzed the composition of prokaryotic communities co-isolated with Leontynka spp. and hypothesize that their preference for hypoxic/microoxic conditions is facilitated by metabolic interactions with certain microaerophilic and anaerobic bacteria. Conclusions This study represents the first comprehensive analysis of microaerophilic Chlamydomonadales algae. Having retained several ancestral enzymes of the anaerobic energy metabolism, Leontynka represents a unique vantage point for understanding the evolution of the hydrogen production machinery and adaptations to low oxygen in Chlamydomonadales (and core chlorophytes in general). Our findings suggest that the plastid of non-photosynthetic Leontynka follows a similar evolutionary path as mitochondria when adapting to anaerobiosis and parallels the transition of a mitochondrion into a hydrogenosome.