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“Lose-to-gain” adaptation to genome decay in the structure of the smallest eukaryotic ribosomes

David Nicholson, View ORCID ProfileMarco Salamina, View ORCID ProfileJohan Panek, Karla Helena-Bueno, View ORCID ProfileCharlotte R. Brown, View ORCID ProfileRobert P. Hirt, View ORCID ProfileNeil A. Ranson, View ORCID ProfileSergey V. Melnikov
doi: https://doi.org/10.1101/2021.09.06.458831
David Nicholson
1Astbury Centre for Structural Molecular Biology, School of Molecular & Cellular Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK
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Marco Salamina
2Biosciences Institute, Newcastle University, Newcastle upon Tyne, NE2 4HH, UK
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Johan Panek
2Biosciences Institute, Newcastle University, Newcastle upon Tyne, NE2 4HH, UK
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Karla Helena-Bueno
2Biosciences Institute, Newcastle University, Newcastle upon Tyne, NE2 4HH, UK
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Charlotte R. Brown
2Biosciences Institute, Newcastle University, Newcastle upon Tyne, NE2 4HH, UK
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Robert P. Hirt
2Biosciences Institute, Newcastle University, Newcastle upon Tyne, NE2 4HH, UK
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Neil A. Ranson
1Astbury Centre for Structural Molecular Biology, School of Molecular & Cellular Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK
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  • For correspondence: n.a.ranson@leeds.ac.uk sergey.melnikov@ncl.ac.uk
Sergey V. Melnikov
2Biosciences Institute, Newcastle University, Newcastle upon Tyne, NE2 4HH, UK
3Faculty of Medical Sciences, Newcastle University, Newcastle upon Tyne, NE2 4HH, UK
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  • For correspondence: n.a.ranson@leeds.ac.uk sergey.melnikov@ncl.ac.uk
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Abstract

The evolution of microbial parasites involves the interplay of two opposing forces. On the one hand, the pressure to survive drives parasites to improve through Darwinian natural selection. On the other, frequent genetic drifts result in genome decay, an evolutionary process in which an ever-increasing burden of deleterious mutations leads to gene loss and gradual genome reduction. Here, seeking to understand how this interplay occurs at the scale of individual macromolecules, we describe cryo-EM and evolutionary analyses of ribosomes from Encephalitozoon cuniculi, a eukaryote with one of the most reduced genomes in nature. We show that E. cuniculi ribosomes, the smallest eukaryotic cytoplasmic ribosomes to be structurally characterized, employ unparalleled structural innovations that allow extreme rRNA reduction without loss of ribosome integrity. These innovations include the evolution of previously unknown rRNA features such as molten rRNA linkers and bulgeless rRNA. Furthermore, we show that E. cuniculi ribosomes withstand the loss of rRNA and protein segments by evolving a unique ability to effectively trap small molecules and use them as ribosomal building-blocks and structural mimics of degenerated rRNA and protein segments. Overall, our work reveals a recurrent evolutionary pattern, which we term “lose-to-gain” evolution, where it is only through the loss of rRNA and protein segments that E. cuniculi ribosomes evolve their major innovations. Our study shows that the molecular structures of intracellular parasites long viewed as reduced, degenerated, and suffering from various debilitating mutations instead possess an array of systematically overlooked and extraordinary structural features. These features allow them to not only adapt to molecular reduction but evolve new activities that parasites can possibly use to their advantage.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://drive.google.com/drive/folders/1Sq3ufbPkJjdiD3AMwmJe6hlSbzlIjrN7?usp=sharing

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 06, 2021.
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“Lose-to-gain” adaptation to genome decay in the structure of the smallest eukaryotic ribosomes
David Nicholson, Marco Salamina, Johan Panek, Karla Helena-Bueno, Charlotte R. Brown, Robert P. Hirt, Neil A. Ranson, Sergey V. Melnikov
bioRxiv 2021.09.06.458831; doi: https://doi.org/10.1101/2021.09.06.458831
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“Lose-to-gain” adaptation to genome decay in the structure of the smallest eukaryotic ribosomes
David Nicholson, Marco Salamina, Johan Panek, Karla Helena-Bueno, Charlotte R. Brown, Robert P. Hirt, Neil A. Ranson, Sergey V. Melnikov
bioRxiv 2021.09.06.458831; doi: https://doi.org/10.1101/2021.09.06.458831

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