Recent Advances in Archaeal Translation Initiation

Abstract

Translation initiation (TI) allows accurate selection of the initiation codon on a messenger RNA (mRNA) and defines the reading frame. In all domains of life, translation initiation generally occurs within a macromolecular complex made up of the small ribosomal subunit, the mRNA, a specialized methionylated initiator tRNA, and translation initiation factors (IFs). Once the start codon is selected at the P site of the ribosome and the large subunit is associated, the IFs are released and a ribosome competent for elongation is formed. However, even if the general principles are the same in the three domains of life, the molecular mechanisms are different in bacteria, eukaryotes, and archaea and may also vary depending on the mRNA. Because TI mechanisms have evolved lately, their studies bring important information about the evolutionary relationships between extant organisms. In this context, recent structural data on ribosomal complexes and genomewide studies are particularly valuable. This review focuses on archaeal translation initiation highlighting its relationships with either the eukaryotic or the bacterial world. Eukaryotic features of the archaeal small ribosomal subunit are presented. Ribosome evolution and TI mechanisms diversity in archaeal branches are discussed. Next, the use of leaderless mRNAs and that of leadered mRNAs having Shine-Dalgarno sequences is analyzed. Finally, the current knowledge on TI mechanisms of SD-leadered and leaderless mRNAs is detailed.

Evolution of the genetic code

“…We posit that genetic code starts and stops were late additions to the code. Translation initiation in Archaea has recently been reviewed [ 101 ]. Archaea utilize Met-tRNA iMet (iMet for initiator methionine) and a set of translation initiation factors.…”

Elucidation of the Translation Initiation Factor Interaction Network of Haloferax volcanii Reveals Coupling of Transcription and Translation in Haloarchaea

“…As mentioned in the Introduction , in recent years considerable progress has been obtained in the analysis of translation initiation in archaea. A very recent review gives an excellent overview of the progress ( Schmitt et al, 2020 ). Breakthrough results were the structure determinations of preinitiation complexes from P. abyssi ( Coureux et al, 2016 , 2020 ).…”

“…In addition, SD motifs are non-functional for translation initiation at 5'-UTRs in H. volcanii ( Kramer et al, 2014 ). Several reviews summarize various aspects about translation initiation in archaea, and compare it with initiation in bacteria and eukaryotes ( Londei, 2005 ; Benelli and Londei, 2009 , 2011 ; Schmitt et al, 2019 , 2020 ).…”

“…A central factor is the heterotrimeric factor aIF2/eIF2, which binds the initiator tRNA and brings it into the P-site of the ribosome. aIF1 and eIF1 are homologous and are found in the preinitiation complex of archaea and eukaryotes together with aIF2/eIF2 and aIF1A/eIF1A, thus enhancing the accuracy of start codon selection ( Schmitt et al, 2020 ). The eukaryotic factor eIF4F consists of three subunits, a homolog of one of which, a/eIF4A, is encoded in many archaeal genomes.…”

“…In recent years considerable progress in the experimental characterization of translation initiation has been obtained, albeit the number of studies is much lower than the number of studies in eukaryotes or in bacteria (in Pubmed the numbers of studies with “translation initiation” AND archae*, bacteri*, or eukaryote* in Title/Abstract are 187, 892, and 4,890, respectively). By far the highest number of studies have been performed with the Crenarchaeon Sulfolobus solfataricus ( La Teana et al, 2013 ; Schmitt et al, 2020 ). Structures of preinitiation complexes have been solved with constituents from Pyrococcus abyssi ( Coureux et al, 2016 , 2020 ).…”