Updated publication reference for PubMed record(s): 30415698. The mitochondrial contact site and cristae organization system (MICOS) is a complex responsible for proper cristae formation. Empirical data about this ubiquitous complex is limited to opisthokont models (e.g. yeast), impeding understanding of its core properties and adaptation potential to diverse cellular milieus. To close this knowledge gap, we characterized MICOS from the diverged excavate Trypanosoma brucei. These results allow the definition of fundamental MICOS properties, such as its role in maintaining both cristae and contacts between the inner and outer membranes plus its extrusion into the intermembrane space. Yet, surprising differences with opisthokonts indicate that MICOS can assume different forms. T. brucei MICOS contains a novel subunit involved in the import of intermembrane space proteins, including respiratory chain complex assembly factors. We propose an evidence-based hypothesis that T. brucei MICOS populates cristae membranes with proteins needed for respiration, supported by the complex's even distribution in cristae