Cryo-EM Structure of the Archaeal 50S Ribosomal Subunit in Complex with Initiation Factor 6 and Implications for Ribosome Evolution

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Abstract

Translation of mRNA into proteins by the ribosome is universally conserved in all cellular life. The composition and complexity of the translation machinery differ markedly between the three domains of life. Organisms from the domain Archaea show an intermediate level of complexity, sharing several additional components of the translation machinery with eukaryotes that are absent in bacteria. One of these translation factors is initiation factor 6 (IF6), which associates with the large ribosomal subunit. We have reconstructed the 50S ribosomal subunit from the archaeon Methanothermobacter thermautotrophicus in complex with archaeal IF6 at 6.6 Å resolution using cryo-electron microscopy (EM). The structure provides detailed architectural insights into the 50S ribosomal subunit from a methanogenic archaeon through identification of the rRNA expansion segments and ribosomal proteins that are shared between this archaeal ribosome and eukaryotic ribosomes but are mostly absent in bacteria and in some archaeal lineages. Furthermore, the structure reveals that, in spite of highly divergent evolutionary trajectories of the ribosomal particle and the acquisition of novel functions of IF6 in eukaryotes, the molecular binding of IF6 on the ribosome is conserved between eukaryotes and archaea. The structure also provides a snapshot of the reductive evolution of the archaeal ribosome and offers new insights into the evolution of the translation system in archaea.

Graphical Abstract

Research Highlights

► The 6.6-Å cryo-EM structure of the archaeal 50S ribosomal subunit in complex with aIF6. ► Highest-resolution cryo-EM reconstruction of an isolated ribosomal subunit. ► Conservation of archaeal and eukaryotic IF6 binding across kingdoms. ► Implications for functional interactions of IF6 with translation factors. ► Structural insight into the reductive evolution of the archaeal ribosome.

Abbreviations

IF6
initiation factor 6
EM
electron microscopy
3D
three-dimensional
PDB
Protein Data Bank
EDTA
ethylenediaminetetraacetic acid

Keywords

ribosome
IF6
cryo-EM
CCD detector
evolution

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Present addresses: V. Godinic-Mikulcic, Department of Chemistry, Faculty of Science, University of Zagreb, Horvatovac 102a, 10 000 Zagreb, Croatia; A. Crnkovic, Department of Chemistry, Faculty of Science, University of Zagreb, Horvatovac 102a, 10 000 Zagreb, Croatia.