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Muller’s Ratchet and ribosome degeneration in the obligate intracellular parasites Microsporidia

Lookup NU author(s): Dr Sergey MelnikovORCiD

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This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


Abstract

© 2018 by the authors. Licensee MDPI, Basel, Switzerland.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.


Publication metadata

Author(s): Melnikov SV, Manakongtreecheep K, Rivera KD, Makarenko A, Pappin DJ, Soll D

Publication type: Article

Publication status: Published

Journal: International Journal of Molecular Sciences

Year: 2018

Volume: 19

Issue: 12

Print publication date: 01/12/2018

Online publication date: 19/12/2018

Acceptance date: 16/12/2018

Date deposited: 28/05/2020

ISSN (print): 1661-6596

ISSN (electronic): 1422-0067

Publisher: MDPI AG

URL: https://doi.org/10.3390/ijms19124125

DOI: 10.3390/ijms19124125

PubMed id: 30572624


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Funding

Funder referenceFunder name
... grant number DE-FG02-98ER20311 (both to D.S.).
Cold Spring Harbor Laboratory Mass Spectrometry Shared Resource, which is supported by the National Cancer Institute Cancer Center Support Grant 5P30CA045508 (to D.J.P.)
funded by the National Institute of General Medical Sciences (NIGMS) at the National Institutes of Health, grant number R35GM122560...

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