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Ciliate mitoribosome illuminates evolutionary steps of mitochondrial translation
Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics. Stockholm University, Science for Life Laboratory (SciLifeLab). Karolinska Institutet, Sweden.
Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics. Stockholm University, Science for Life Laboratory (SciLifeLab). Karolinska Institutet, Sweden.ORCID iD: 0000-0002-5302-1740
Number of Authors: 22020 (English)In: eLIFE, E-ISSN 2050-084X, Vol. 9, article id e59264Article in journal (Refereed) Published
Abstract [en]

To understand the steps involved in the evolution of translation, we used Tetrahymena thermophila, a ciliate with high coding capacity of the mitochondrial genome, as the model organism and characterized its mitochondrial ribosome (mitoribosome) using cryo-EM. The structure of the mitoribosome reveals an assembly of 94-ribosomal proteins and four-rRNAs with an additional protein mass of ~700 kDa on the small subunit, while the large subunit lacks 5S rRNA. The structure also shows that the small subunit head is constrained, tRNA binding sites are formed by mitochondria-specific protein elements, conserved protein bS1 is excluded, and bacterial RNA polymerase binding site is blocked. We provide evidence for anintrinsic protein targeting system through visualization of mitochondria-specific mL105 by the exit tunnel that would facilitate the recruitment of a nascent polypeptide. Functional protein uS3m is encoded by three complementary genes from the nucleus and mitochondrion, establishing a link between genetic drift and mitochondrial translation. Finally, we reannotated nine open reading frames in the mitochondrial genome that code for mitoribosomal proteins.

Place, publisher, year, edition, pages
2020. Vol. 9, article id e59264
Keywords [en]
sequence, subunit, RNA, visualization, alignment, protein, genome
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:su:diva-184592DOI: 10.7554/eLife.59264ISI: 000545981800001PubMedID: 32553108Scopus ID: 2-s2.0-85087465791OAI: oai:DiVA.org:su-184592DiVA, id: diva2:1462758
Funder
Ragnar Söderbergs stiftelse, M44/16Swedish Cancer Society, 2017/1041Knut and Alice Wallenberg Foundation, 2018.0080Swedish Foundation for Strategic Research, FFL15:0325Swedish Research Council, NT_2015–04107Available from: 2020-08-31 Created: 2020-08-31 Last updated: 2022-08-26Bibliographically approved
In thesis
1. On the Origin and Evolution of the Mitochondrial Ribosome
Open this publication in new window or tab >>On the Origin and Evolution of the Mitochondrial Ribosome
2022 (English)Doctoral thesis, comprehensive summary (Other academic)
Alternative title[sv]
Den mitokondriella ribosomens ursprung och utveckling
Abstract [en]

The ribosome is among the most ancient, intricate and well studied macromolecular complexes in biology. Predating the earliest divergence of life, its core molecular structure has remained mostly unchanged for more than three billion years. In stark contrast to its monolithic ancestor, the mitochondrial ribosome represents one of the most architecturally diverse protein complexes investigated. This work is an attempt at reconciling these two paradigms. In this thesis I first briefly cover the evolutionary history of the mitochondrial ribosome: from its ancient origins, through the process of Eukaryogenesis and the development of mitochondria, to its current state. Following this I present a comprehensive and integrated comparative analysis of the current mitoribosomal structures. Using these structural observations as a starting point I then summarise the current knowledge regarding the evolutionary trends of mitochondrial ribosomes. Finally I review and discuss potential genetic mechanisms and evolutionary pressures which could have produced such a vibrant diversity of structures. Together with this analysis I present monosome structures from the ciliate Tetrahymena thermophila and chlorophycean Polytomella magna together with an assembly intermediate of the large subunit from Trypanosoma brucei. Together, I hope to demonstrate the impact of the unique mitochondrial environment on the evolution of the mitochondrial ribosome. 

Place, publisher, year, edition, pages
Stockholm: Department of Biochemistry and Biophysics, Stockholm University, 2022. p. 86
Keywords
Ribosome, mitochondria, evolution, structural biology
National Category
Biochemistry Molecular Biology
Research subject
Biochemistry
Identifiers
urn:nbn:se:su:diva-203931 (URN)978-91-7911-878-5 (ISBN)978-91-7911-879-2 (ISBN)
Public defence
2022-05-20, Magnélisalen, Kemiska övningslaboratoriet, Svante Arrhenius väg 16 B, Stockholm, 13:30 (English)
Opponent
Supervisors
Available from: 2022-04-27 Created: 2022-04-15 Last updated: 2025-02-20Bibliographically approved

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Tobiasson, VictorAmunts, Alexey

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