Abstract
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.
Highlights
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
How do parasites retain the function of their molecular machines in the face of extreme genome reduction? Our study provides answers to this question by describing a complex molecular structure—the ribosome—from E. cuniculi, an organism with one of the smallest eukaryotic genomes
Ribosomes from organisms with small genomes, including many intracellular parasites and endosymbionts, were predicted to lack multiple ribosomal proteins and up to a third of rRNA nucleotides compared to free-living species[27,29,30,49]
Summary
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. In a process known as genome decay, microbial parasites accumulate deleterious mutations that transform many formerly essential genes into pseudogenes, leading to gradual gene loss and mutational meltdown[14,15] This meltdown can eliminate up to ∼95% of genes in the most ancient intracellular organisms compared to closely related free-living species[16–18]. Because parasites live in small, asexual and genetically bottle-necked populations, they cannot effectively eliminate deleterious mutations that sporadically occur during DNA replication This causes irreversible accumulation of deleterious mutations and reduction of parasite genomes[18]. It is not that parasites lose only those genes that are no longer essential for their survival in the intracellular context It is that parasites populations cannot effectively eliminate sporadic deleterious mutations, causing accumulation of these mutations throughout their genomes, including their most essential genes[10–13]. We know little about the impact of intracellular lifestyles on all other properties of cellular macromolecules, including molecular adaptations to the everincreasing burden of deleterious mutations
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