Coevolution of the translational machinery optimizes initiation with unusual initiator tRNAs and initiation codons in mycoplasmas

Ayyub, Shreya Ahana; Dobriyal, Divya; Shah, Riyaz Ahmad; Lahry, Kuldeep; Bhattacharyya, Madhumita; Bhattacharyya, Souvik; Chakrabarti, Saikat; Varshney, Umesh

doi:10.1080/15476286.2017.1377879

Cited by 8 publications

(11 citation statements)

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“…7c). The present observations in the archaeal system agree with previous studies in E. coli showing that the central GC pair and particularly base G30 was the most crucial nucleotide for translation fidelity [64][65][66] .…”

Section: Discussionsupporting

confidence: 93%

Cryo-EM study of an archaeal 30S initiation complex gives insights into evolution of translation initiation

et al. 2020

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Archaeal translation initiation occurs within a macromolecular complex containing the small ribosomal subunit (30S) bound to mRNA, initiation factors aIF1, aIF1A and the ternary complex aIF2:GDPNP:Met-tRNA i Met. Here, we determine the cryo-EM structure of a 30S: mRNA:aIF1A:aIF2:GTP:Met-tRNA i Met complex from Pyrococcus abyssi at 3.2 Å resolution. It highlights archaeal features in ribosomal proteins and rRNA modifications. We find an aS21 protein, at the location of eS21 in eukaryotic ribosomes. Moreover, we identify an N-terminal extension of archaeal eL41 contacting the P site. We characterize 34 N 4-acetylcytidines distributed throughout 16S rRNA, likely contributing to hyperthermostability. Without aIF1, the 30S head is stabilized and initiator tRNA is tightly bound to the P site. A network of interactions involving tRNA, mRNA, rRNA modified nucleotides and C-terminal tails of uS9, uS13 and uS19 is observed. Universal features and domain-specific idiosyncrasies of translation initiation are discussed in light of ribosomal structures from representatives of each domain of life.

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Section: Discussionsupporting

confidence: 93%

Cryo-EM study of an archaeal 30S initiation complex gives insights into evolution of translation initiation

et al. 2020

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“…The uS12 and IF3 do not directly interact with each other in SSU (Figure 2a) (Hussain et al., 2016). However, our earlier studies suggested the possibility of coevolution of variations in uS9, IF3 and uS12 proteins of the translation machinery in mycoplasma species harboring variations in the 3GC region of the i‐tRNA (Figure ) (Ayyub et al., 2018a).…”

Section: Resultsmentioning

confidence: 99%

“…To advance our understanding of the significance of the infC V93A mutation in the suppressors, we utilized a well characterized infC135 allele of IF3 bearing the mutation Arg131Pro, which is known to, (a) confer errors in start codon discrimination, (b) allow initiation with non‐3GC bp containing i‐tRNAs, (c) possess altered binding efficiency to the ribosomes, and (d) exhibit a loss of autoregulation of IF3 from its AUU start codon (Haggerty & Lovett, 1993, 1997; O’Connor et al., 2001). Interestingly, the Arg131Pro variation is naturally found in IF3 in mycoplasma possessing the au/GC/Gu variant i‐tRNA and has been shown to play an important role in accommodation of the variant i‐tRNA in the ribosome (Ayyub et al., 2018a). We transduced DK‐GC/GC/GC, DK‐cg/GC/cg, Sup‐1 and Sup‐2 strains with the infC135 allele (Figure 6a(i)) and checked its effects on the growth.…”

Section: Resultsmentioning

confidence: 99%

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Systematic evolution of initiation factor 3 and the ribosomal protein uS12 optimizes Escherichia coli growth with an unconventional initiator tRNA

Datta

Singh

Modak

et al. 2021

Molecular Microbiology

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The anticodon stem of initiator tRNA (i‐tRNA) possesses the characteristic three consecutive GC base pairs (G29:C41, G30:C40, and G31:C39 abbreviated as GC/GC/GC or 3GC pairs) crucial to commencing translation. To understand the importance of this highly conserved element, we isolated two fast‐growing suppressors of Escherichia coli sustained solely on an unconventional i‐tRNA (i‐tRNAcg/GC/cg) having cg/GC/cg sequence instead of the conventional GC/GC/GC. Both suppressors have the common mutation of V93A in initiation factor 3 (IF3), and additional mutations of either V32L (Sup‐1) or H76L (Sup‐2) in small subunit ribosomal protein 12 (uS12). The V93A mutation in IF3 was necessary for relaxed fidelity of i‐tRNA selection to sustain on i‐tRNAcg/GC/cg though with a retarded growth. Subsequent mutations in uS12 salvaged the retarded growth by enhancing the fidelity of translation. The H76L mutation in uS12 showed better fidelity of i‐tRNA selection. However, the V32L mutation compensated for the deficient fidelity of i‐tRNA selection by ensuring an efficient fidelity check by ribosome recycling factor (RRF). We reveal unique genetic networks between uS12, IF3 and i‐tRNA in initiation and between uS12, elongation factor‐G (EF‐G), RRF, and Pth (peptidyl‐tRNA hydrolase) which, taken together, govern the fidelity of translation in bacteria.

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“…Concerning uS13 and uS19, the C-tails of these two proteins are oriented toward the major groove of the anticodon stem of the initiator tRNA (Figure 7). In particular, they interact with G30 of the second base pair of the almost universally conserved three GC base pairs of the anticodon stem of the initiator tRNA, that play a crucial role in translation fidelity (Samhita et al, 2012;Hussain et al, 2016;Shetty et al, 2017;Ayyub et al, 2018). Sequence alignments of uS13 showed that the basic character of the C-tail is conserved in the three domains of life.…”

Section: Three Universal Proteins Participate In the Selection Of Thementioning

confidence: 99%

Recent Advances in Archaeal Translation Initiation

et al. 2020

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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.

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Coevolution of the translational machinery optimizes initiation with unusual initiator tRNAs and initiation codons in mycoplasmas

Cited by 8 publications

References 40 publications

Cryo-EM study of an archaeal 30S initiation complex gives insights into evolution of translation initiation

Cryo-EM study of an archaeal 30S initiation complex gives insights into evolution of translation initiation

Systematic evolution of initiation factor 3 and the ribosomal protein uS12 optimizes Escherichia coli growth with an unconventional initiator tRNA

Recent Advances in Archaeal Translation Initiation

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