Abstract

Mitochondrial ribosomes (mitoribosomes) are essential, and their function of synthesising mitochondrial proteins is universal. The core of almost all mitoribosomes is formed from a small number of long and self-folding rRNA molecules. In contrast, the mitoribosome of the apicomplexan parasite Toxoplasma gondii assembles from over 50 extremely short rRNA molecules. We used cryo-EM structural analysis in combination with genetics and cell biology to discover the features that enable this unusual mitoribosome to perform its function. Our studies revealed novel ribosome features that mitigate this extreme fragmentation, including a new role for Poly-A tails and abundant repurposing of proteins with other functional domains. We further provide evidence for mitoribosome adaptation to the mitochondrial genome irregularities found in T. gondii. Altogether, Toxoplasma’s unusual biology provided us with a magnifying glass to understand new principles of mitoribosomes biology and function.