Types and Functions of Mitoribosome-Specific Ribosomal Proteins Across Eukaryotes

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2022 Apr 12

PMID 35408834

Authors

Vassilis Scaltsoyiannes

Nicolas Corre

Florent Waltz

Philippe Giege

Affiliations

Soon will be listed here.

Abstract

Mitochondria are key organelles that combine features inherited from their bacterial endosymbiotic ancestor with traits that arose during eukaryote evolution. These energy producing organelles have retained a genome and fully functional gene expression machineries including specific ribosomes. Recent advances in cryo-electron microscopy have enabled the characterization of a fast-growing number of the low abundant membrane-bound mitochondrial ribosomes. Surprisingly, mitoribosomes were found to be extremely diverse both in terms of structure and composition. Still, all of them drastically increased their number of ribosomal proteins. Interestingly, among the more than 130 novel ribosomal proteins identified to date in mitochondria, most of them are composed of a-helices. Many of them belong to the nuclear encoded super family of helical repeat proteins. Here we review the diversity of functions and the mode of action held by the novel mitoribosome proteins and discuss why these proteins that share similar helical folds were independently recruited by mitoribosomes during evolution in independent eukaryote clades.

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References

Ben-Shem A, Garreau de Loubresse N, Melnikov S, Jenner L, Yusupova G, Yusupov M . The structure of the eukaryotic ribosome at 3.0 Å resolution. Science. 2011; 334(6062):1524-9. DOI: 10.1126/science.1212642. View

Desai N, Brown A, Amunts A, Ramakrishnan V . The structure of the yeast mitochondrial ribosome. Science. 2017; 355(6324):528-531. PMC: 5295643. DOI: 10.1126/science.aal2415. View

De Silva D, Tu Y, Amunts A, Fontanesi F, Barrientos A . Mitochondrial ribosome assembly in health and disease. Cell Cycle. 2015; 14(14):2226-50. PMC: 4615001. DOI: 10.1080/15384101.2015.1053672. View

Valach M, Gonzalez Alcazar J, Sarrasin M, Lang B, Gray M, Burger G . An Unexpectedly Complex Mitoribosome in Andalucia godoyi, a Protist with the Most Bacteria-like Mitochondrial Genome. Mol Biol Evol. 2020; 38(3):788-804. PMC: 7947838. DOI: 10.1093/molbev/msaa223. View

Ott M, Prestele M, Bauerschmitt H, Funes S, Bonnefoy N, Herrmann J . Mba1, a membrane-associated ribosome receptor in mitochondria. EMBO J. 2006; 25(8):1603-10. PMC: 1440829. DOI: 10.1038/sj.emboj.7601070. View

Waltz F, Corre N, Hashem Y, Giege P . Specificities of the plant mitochondrial translation apparatus. Mitochondrion. 2020; 53:30-37. DOI: 10.1016/j.mito.2020.04.008. View

Bjorkholm P, Harish A, Hagstrom E, Ernst A, Andersson S . Mitochondrial genomes are retained by selective constraints on protein targeting. Proc Natl Acad Sci U S A. 2015; 112(33):10154-61. PMC: 4547212. DOI: 10.1073/pnas.1421372112. View

Smirnov A, Forstner K, Holmqvist E, Otto A, Gunster R, Becher D . Grad-seq guides the discovery of ProQ as a major small RNA-binding protein. Proc Natl Acad Sci U S A. 2016; 113(41):11591-11596. PMC: 5068311. DOI: 10.1073/pnas.1609981113. View

Cipullo M, Valentin Gese G, Khawaja A, Hallberg B, Rorbach J . Structural basis for late maturation steps of the human mitoribosomal large subunit. Nat Commun. 2021; 12(1):3673. PMC: 8209036. DOI: 10.1038/s41467-021-23617-8. View

10.

Khatter H, Myasnikov A, Natchiar S, Klaholz B . Structure of the human 80S ribosome. Nature. 2015; 520(7549):640-5. DOI: 10.1038/nature14427. View

11.

Teramoto T, Kaitany K, Kakuta Y, Kimura M, Fierke C, Hall T . Pentatricopeptide repeats of protein-only RNase P use a distinct mode to recognize conserved bases and structural elements of pre-tRNA. Nucleic Acids Res. 2020; 48(21):11815-11826. PMC: 7708040. DOI: 10.1093/nar/gkaa627. View

12.

Aphasizheva I, Maslov D, Wang X, Huang L, Aphasizhev R . Pentatricopeptide repeat proteins stimulate mRNA adenylation/uridylation to activate mitochondrial translation in trypanosomes. Mol Cell. 2011; 42(1):106-17. PMC: 3073060. DOI: 10.1016/j.molcel.2011.02.021. View

13.

Adl S, Bass D, Lane C, Lukes J, Schoch C, Smirnov A . Revisions to the Classification, Nomenclature, and Diversity of Eukaryotes. J Eukaryot Microbiol. 2018; 66(1):4-119. PMC: 6492006. DOI: 10.1111/jeu.12691. View

14.

Londei P, Ferreira-Cerca S . Ribosome Biogenesis in Archaea. Front Microbiol. 2021; 12:686977. PMC: 8339473. DOI: 10.3389/fmicb.2021.686977. View

15.

Nikolay R, Hilal T, Schmidt S, Qin B, Schwefel D, Vieira-Vieira C . Snapshots of native pre-50S ribosomes reveal a biogenesis factor network and evolutionary specialization. Mol Cell. 2021; 81(6):1200-1215.e9. DOI: 10.1016/j.molcel.2021.02.006. View

16.

Sissler M, Hashem Y . Mitoribosome assembly comes into view. Nat Struct Mol Biol. 2021; 28(8):631-633. DOI: 10.1038/s41594-021-00640-3. View

17.

Borst P, Grivell L . Mitochondrial ribosomes. FEBS Lett. 1971; 13(2):73-88. DOI: 10.1016/0014-5793(71)80204-1. View

18.

Allen J . Why chloroplasts and mitochondria retain their own genomes and genetic systems: Colocation for redox regulation of gene expression. Proc Natl Acad Sci U S A. 2015; 112(33):10231-8. PMC: 4547249. DOI: 10.1073/pnas.1500012112. View

19.

Ojala D, Montoya J, Attardi G . tRNA punctuation model of RNA processing in human mitochondria. Nature. 1981; 290(5806):470-4. DOI: 10.1038/290470a0. View

20.

Lau B, Cheng J, Flemming D, La Venuta G, Berninghausen O, Beckmann R . Structure of the Maturing 90S Pre-ribosome in Association with the RNA Exosome. Mol Cell. 2020; 81(2):293-303.e4. DOI: 10.1016/j.molcel.2020.11.009. View