Evolution of the Protein Stoichiometry in the L12 Stalk of Bacterial and Organellar Ribosomes

Overview

Journal Nat Commun

Specialty Biology

Date 2013 Jan 24

PMID 23340427

Citations 24

Authors

Iakov I Davydov

Ingo Wohlgemuth

Irena I Artamonova

Henning Urlaub

Alexander G Tonevitsky

Marina V Rodnina

Affiliations

Soon will be listed here.

Abstract

The emergence of ribosomes and translation factors is central for understanding the origin of life. Recruitment of translation factors to bacterial ribosomes is mediated by the L12 stalk composed of protein L10 and several copies of protein L12, the only multi-copy protein of the ribosome. Here we predict stoichiometries of L12 stalk for >1,200 bacteria, mitochondria and chloroplasts by a computational analysis, and validate the predictions by quantitative mass spectrometry. The majority of bacteria have L12 stalks allowing for binding of four or six copies of L12, largely independent of the taxonomic group or living conditions of the bacteria, whereas some cyanobacteria have eight copies. Mitochondrial and chloroplast ribosomes can accommodate six copies of L12. The last universal common ancestor probably had six molecules of L12 molecules bound to L10. Changes of the stalk composition provide a unique possibility to trace the evolution of protein components of the ribosome.

Citing Articles

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References

Talavera G, Castresana J . Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007; 56(4):564-77. DOI: 10.1080/10635150701472164. View

Robertson M, Joyce G . The origins of the RNA world. Cold Spring Harb Perspect Biol. 2010; 4(5). PMC: 3331698. DOI: 10.1101/cshperspect.a003608. View

Ilag L, Videler H, McKay A, Sobott F, Fucini P, Nierhaus K . Heptameric (L12)6/L10 rather than canonical pentameric complexes are found by tandem MS of intact ribosomes from thermophilic bacteria. Proc Natl Acad Sci U S A. 2005; 102(23):8192-7. PMC: 1149426. DOI: 10.1073/pnas.0502193102. View

Yarza P, Richter M, Peplies J, Euzeby J, Amann R, Schleifer K . The All-Species Living Tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol. 2008; 31(4):241-50. DOI: 10.1016/j.syapm.2008.07.001. View

Huelsenbeck J, Ronquist F . MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001; 17(8):754-5. DOI: 10.1093/bioinformatics/17.8.754. View

Hamel E, Koka M, Nakamoto T . Requirement of an Escherichia coli 50 S ribosomal protein component for effective interaction of the ribosome with T and G factors and with guanosine triphosphate. J Biol Chem. 1972; 247(3):805-14. View

Helgstrand M, Mandava C, Mulder F, Liljas A, Sanyal S, Akke M . The ribosomal stalk binds to translation factors IF2, EF-Tu, EF-G and RF3 via a conserved region of the L12 C-terminal domain. J Mol Biol. 2006; 365(2):468-79. DOI: 10.1016/j.jmb.2006.10.025. View

Gordiyenko Y, Videler H, Zhou M, McKay A, Fucini P, Biegel E . Mass spectrometry defines the stoichiometry of ribosomal stalk complexes across the phylogenetic tree. Mol Cell Proteomics. 2010; 9(8):1774-83. PMC: 2938062. DOI: 10.1074/mcp.M000072-MCP201. View

Ban N, Nissen P, Hansen J, Moore P, Steitz T . The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science. 2000; 289(5481):905-20. DOI: 10.1126/science.289.5481.905. View

10.

Ronquist F, Huelsenbeck J . MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003; 19(12):1572-4. DOI: 10.1093/bioinformatics/btg180. View

11.

. Ongoing and future developments at the Universal Protein Resource. Nucleic Acids Res. 2010; 39(Database issue):D214-9. PMC: 3013648. DOI: 10.1093/nar/gkq1020. View

12.

Picotti P, Aebersold R . Selected reaction monitoring-based proteomics: workflows, potential, pitfalls and future directions. Nat Methods. 2012; 9(6):555-66. DOI: 10.1038/nmeth.2015. View

13.

Gray M, Burger G, Lang B . The origin and early evolution of mitochondria. Genome Biol. 2001; 2(6):REVIEWS1018. PMC: 138944. DOI: 10.1186/gb-2001-2-6-reviews1018. View

14.

Beringer M, Rodnina M . The ribosomal peptidyl transferase. Mol Cell. 2007; 26(3):311-21. DOI: 10.1016/j.molcel.2007.03.015. View

15.

Wahl M, Moller W . Structure and function of the acidic ribosomal stalk proteins. Curr Protein Pept Sci. 2002; 3(1):93-106. DOI: 10.2174/1389203023380756. View

16.

Kirkpatrick D, Gerber S, Gygi S . The absolute quantification strategy: a general procedure for the quantification of proteins and post-translational modifications. Methods. 2005; 35(3):265-73. DOI: 10.1016/j.ymeth.2004.08.018. View

17.

Spahn C, Gomez-Lorenzo M, Grassucci R, Jorgensen R, Andersen G, Beckmann R . Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J. 2004; 23(5):1008-19. PMC: 380967. DOI: 10.1038/sj.emboj.7600102. View

18.

Brot N, Tate W, Caskey C, Weissbach H . The requirement for ribosomal proteins L7 and L12 in peptide-chain termination. Proc Natl Acad Sci U S A. 1974; 71(1):89-92. PMC: 387938. DOI: 10.1073/pnas.71.1.89. View

19.

Rodnina M, Wintermeyer W . GTP consumption of elongation factor Tu during translation of heteropolymeric mRNAs. Proc Natl Acad Sci U S A. 1995; 92(6):1945-9. PMC: 42399. DOI: 10.1073/pnas.92.6.1945. View

20.

Jones D . Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol. 1999; 292(2):195-202. DOI: 10.1006/jmbi.1999.3091. View