Abstract
Microsporidia are fungi-like parasites that have the smallest known eukaryotic genome, and for that reason they are used as a model to study the phenomenon of genome decay in parasitic forms of life. Similar to other intracellular parasites that reproduce asexually in an environment with alleviated natural selection, Microsporidia experience continuous genome decay that is driven by Muller’s ratchet—an evolutionary process of irreversible accumulation of deleterious mutations that lead to gene loss and the miniaturization of cellular components. Particularly, Microsporidia have remarkably small ribosomes in which the rRNA is reduced to the minimal enzymatic core. In this study, we analyzed microsporidian ribosomes to study an apparent impact of Muller’s ratchet on structure of RNA and protein molecules in parasitic forms of life. Through mass spectrometry of microsporidian proteome and analysis of microsporidian genomes, we found that massive rRNA reduction in microsporidian ribosomes appears to annihilate the binding sites for ribosomal proteins eL8, eL27, and eS31, suggesting that these proteins are no longer bound to the ribosome in microsporidian species. We then provided an evidence that protein eS31 is retained in Microsporidia due to its non-ribosomal function in ubiquitin biogenesis. Our study illustrates that, while Microsporidia carry the same set of ribosomal proteins as non-parasitic eukaryotes, some ribosomal proteins are no longer participating in protein synthesis in Microsporidia and they are preserved from genome decay by having extra-ribosomal functions. More generally, our study shows that many components of parasitic cells, which are identified by automated annotation of pathogenic genomes, may lack part of their biological functions due to continuous genome decay.
Highlights
It is well documented that the parasitic lifestyle causes continuous genome decay, manifested in progressive gene loss and accumulation of deleterious mutations in essential genes [1,2,3]
Mapping of rRNA deletions on the three-dimensional (3D) ribosome structure showed that microsporidian ribosomes lack a few conserved rRNA segments, including helices h15, h16, h17, and h33 in the 18S rRNA, which are otherwise conserved in species from bacteria to eukaryotes (Figure 1A)
Deletions in rRNA in microsporidian ribosomes occur on the ribosome suface, where rRNA expansions extensively interact with ribosomal proteins (Figure 1A,B)
Summary
It is well documented that the parasitic lifestyle causes continuous genome decay, manifested in progressive gene loss and accumulation of deleterious mutations in essential genes [1,2,3]. Among numerous forms of life that inhabit our planet, there is a group of single-cell pathogens that can grow and reproduce only inside other living cells. These organisms evolve under conditions that are radically different from those of free-living species: they live in small population with little competition for nutrients and shelter, which weakens natural selection; they undergo repeated population bottlenecks upon transition from one host cell to another, which favors genetic drifts; and, they proliferate asexually, which prevents the elimination of toxic mutations through recombination of genetic material [3]. In the long-term, this irreversible process, known as Muller’s ratchet, causes genome decay that is reflected in the massive loss of non-essential genes and an increasing number of deleterious mutations in essential genes in parasite genomes [3,4]
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