Cryo-EM Structure of the Highly Atypical Cytoplasmic Ribosome of Euglena Gracilis

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2020 Oct 22

PMID 33091122

Citations 15

Authors

Donna Matzov

Masato Taoka

Yuko Nobe

Yoshio Yamauchi

Yehuda Halfon

Nofar Asis

Ella Zimermann

Haim Rozenberg

Anat Bashan

Shashi Bhushan

Toshiaki Isobe

Michael W Gray

Ada Yonath

Moran Shalev-Benami

Affiliations

Soon will be listed here.

Abstract

Ribosomal RNA is the central component of the ribosome, mediating its functional and architectural properties. Here, we report the cryo-EM structure of a highly divergent cytoplasmic ribosome from the single-celled eukaryotic alga Euglena gracilis. The Euglena large ribosomal subunit is distinct in that it contains 14 discrete rRNA fragments that are assembled non-covalently into the canonical ribosome structure. The rRNA is substantially enriched in post-transcriptional modifications that are spread far beyond the catalytic RNA core, contributing to the stabilization of this highly fragmented ribosome species. A unique cluster of five adenosine base methylations is found in an expansion segment adjacent to the protein exit tunnel, such that it is positioned for interaction with the nascent peptide. As well as featuring distinctive rRNA expansion segments, the Euglena ribosome contains four novel ribosomal proteins, localized to the ribosome surface, three of which do not have orthologs in other eukaryotes.

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References

Shalev-Benami M, Zhang Y, Rozenberg H, Nobe Y, Taoka M, Matzov D . Atomic resolution snapshot of Leishmania ribosome inhibition by the aminoglycoside paromomycin. Nat Commun. 2017; 8(1):1589. PMC: 5693986. DOI: 10.1038/s41467-017-01664-4. View

Kucukelbir A, Sigworth F, Tagare H . Quantifying the local resolution of cryo-EM density maps. Nat Methods. 2013; 11(1):63-5. PMC: 3903095. DOI: 10.1038/nmeth.2727. View

Sharma S, Watzinger P, Kotter P, Entian K . Identification of a novel methyltransferase, Bmt2, responsible for the N-1-methyl-adenosine base modification of 25S rRNA in Saccharomyces cerevisiae. Nucleic Acids Res. 2013; 41(10):5428-43. PMC: 3664796. DOI: 10.1093/nar/gkt195. View

Afonine P, Poon B, Read R, Sobolev O, Terwilliger T, Urzhumtsev A . Real-space refinement in PHENIX for cryo-EM and crystallography. Acta Crystallogr D Struct Biol. 2018; 74(Pt 6):531-544. PMC: 6096492. DOI: 10.1107/S2059798318006551. View

Fischer N, Neumann P, Konevega A, Bock L, Ficner R, Rodnina M . Structure of the E. coli ribosome-EF-Tu complex at <3 Å resolution by Cs-corrected cryo-EM. Nature. 2015; 520(7548):567-70. DOI: 10.1038/nature14275. View

PERRY R . Processing of RNA. Annu Rev Biochem. 1976; 45:605-29. DOI: 10.1146/annurev.bi.45.070176.003133. View

Brito Querido J, Mancera-Martinez E, Vicens Q, Bochler A, Chicher J, Simonetti A . The cryo-EM Structure of a Novel 40S Kinetoplastid-Specific Ribosomal Protein. Structure. 2017; 25(12):1785-1794.e3. DOI: 10.1016/j.str.2017.09.014. View

Ramakrishnan V, White S . Ribosomal protein structures: insights into the architecture, machinery and evolution of the ribosome. Trends Biochem Sci. 1998; 23(6):208-12. DOI: 10.1016/s0968-0004(98)01214-6. View

Bieri P, Leibundgut M, Saurer M, Boehringer D, Ban N . The complete structure of the chloroplast 70S ribosome in complex with translation factor pY. EMBO J. 2016; 36(4):475-486. PMC: 5694952. DOI: 10.15252/embj.201695959. View

10.

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

11.

Taoka M, Nobe Y, Yamaki Y, Sato K, Ishikawa H, Izumikawa K . Landscape of the complete RNA chemical modifications in the human 80S ribosome. Nucleic Acids Res. 2018; 46(18):9289-9298. PMC: 6182160. DOI: 10.1093/nar/gky811. View

12.

Jomaa A, Hwang Fu Y, Boehringer D, Leibundgut M, Shan S, Ban N . Structure of the quaternary complex between SRP, SR, and translocon bound to the translating ribosome. Nat Commun. 2017; 8:15470. PMC: 5454536. DOI: 10.1038/ncomms15470. View

13.

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

14.

Williams C, Headd J, Moriarty N, Prisant M, Videau L, Deis L . MolProbity: More and better reference data for improved all-atom structure validation. Protein Sci. 2017; 27(1):293-315. PMC: 5734394. DOI: 10.1002/pro.3330. View

15.

Wilson D, Cate J . The structure and function of the eukaryotic ribosome. Cold Spring Harb Perspect Biol. 2012; 4(5). PMC: 3331703. DOI: 10.1101/cshperspect.a011536. View

16.

Yokoyama S, Watanabe K, Miyazawa T . Dynamic structures and functions of transfer ribonucleic acids from extreme thermophiles. Adv Biophys. 1987; 23:115-47. DOI: 10.1016/0065-227x(87)90006-2. View

17.

Safra M, Sas-Chen A, Nir R, Winkler R, Nachshon A, Bar-Yaacov D . The m1A landscape on cytosolic and mitochondrial mRNA at single-base resolution. Nature. 2017; 551(7679):251-255. DOI: 10.1038/nature24456. View

18.

Gao J, Duan Z, Zhang L, Huang X, Long L, Tu J . Failure recovery of circulating NKG2DCD56NK cells in HBV-associated hepatocellular carcinoma after hepatectomy predicts early recurrence. Oncoimmunology. 2016; 5(1):e1048061. PMC: 4760296. DOI: 10.1080/2162402X.2015.1048061. View

19.

Lorenz C, Lunse C, Morl M . tRNA Modifications: Impact on Structure and Thermal Adaptation. Biomolecules. 2017; 7(2). PMC: 5485724. DOI: 10.3390/biom7020035. View

20.

Pettersen E, Goddard T, Huang C, Couch G, Greenblatt D, Meng E . UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem. 2004; 25(13):1605-12. DOI: 10.1002/jcc.20084. View