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 genome-wide 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.
Highlights
Translation initiation (TI) allows accurate selection of the initiation codon on a messenger RNA, which defines the reading frame of the protein to be synthesized
At the level of the SSU, this common core corresponds to 90% of bacterial rRNA and encompasses the decoding center of the small ribosomal subunit with in particular the 530 loop and the 1,490 region (Escherichia coli numbering) but not the 3' end corresponding to the messenger RNA (mRNA) exit region
Several studies have shown that in some non-canonical cases, eukaryotic translation initiation used eIF5B instead of eIF2 for the recruitment of the initiator tRNA (Terenin et al, 2008; Thakor and Holcik, 2012; Ho et al, 2018; Ross et al, 2018). This argues in favor of an ancestral translation initiation mechanism involving e/aIF5B/initiation factor 2 (IF2) and e/ aIF1A/IF1 that could have been used in the last common universal ancestor (LUCA) and that should be discussed in the light of what is known for translation initiation of leaderless mRNAs (Londei, 2005; Beck and Moll, 2018)
Summary
Emmanuelle Schmitt*, Pierre-Damien Coureux, Ramy Kazan, Gabrielle Bourgeois, Christine Lazennec-Schurdevin and Yves Mechulam. 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). 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 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 valuable. Eukaryotic features of the archaeal small ribosomal subunit are presented. The current knowledge on TI mechanisms of SD-leadered and leaderless mRNAs is detailed
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