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The evolution of microbial parasites involves the counterplay between natural selection forcing parasites to improve and genetic drifts forcing parasites to lose genes and accumulate deleterious mutations. Here, to understand how this counterplay occurs at the scale of individual macromolecules, we describe cryo-EM structure of ribosomes from  Encephalitozoon cuniculi , a eukaryote with one of the smallest genomes in nature. The extreme rRNA reduction in  E. cuniculi  ribosomes is accompanied with unparalleled structural changes, such as the evolution of previously unknown molten rRNA linkers and bulgeless rRNA. Furthermore,  E. cuniculi  ribosomes withstand the loss of rRNA and protein segments by evolving an ability to use small molecules as structural mimics of degenerated rRNA and protein segments. Overall, we show that the molecular structures long viewed as reduced, degenerated, and suffering from debilitating mutations possess an array of compensatory mechanisms that allow them to remain active despite the extreme molecular reduction.

Adaptation to genome decay in the structure of the smallest eukaryotic ribosome