Co-variation of tRNA Abundance and Codon Usage inEscherichia coliat Different Growth Rates

Dong, H. Henry; Nilsson, Lars; Kurland, C. G.

doi:10.1006/jmbi.1996.0428

Cited by 756 publications

(916 citation statements)

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“…Thus, we propose that the levels of components of the translational apparatus are not only co-regulated at the level of their synthesis, 5,9,93,96,97 but that the level of actively translating ribosomes indirectly regulates the tRNA pool, via degradation of the unengaged tRNAs. Importantly, to maintain a reasonable translation elongation rate even at very low concentrations of active ribosomes, we propose that their association with other protein factors, in particular the abundant elongation factor Tu, would protect a sizable fraction of the tRNA and thereby set a lower bound on the cellular concentration of ternary complexes.…”

Section: Discussionmentioning

confidence: 99%

“…In support of this expectation, Kurland and colleagues measured tRNA concentrations under different growth conditions and found that, indeed, individual tRNA abundances vary with growth rate, albeit modestly, in a manner that reflects the codon frequencies in the corresponding mRNA pools. 5 In addition, there is evidence that an imbalance in the levels of competing charged tRNAs can compromise the fidelity of protein synthesis. 6-8 …”

Section: Introductionmentioning

confidence: 99%

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Transfer RNA instability as a stress response inEscherichia coli: Rapid dynamics of the tRNA pool as a function of demand

2018

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Production of the translation apparatus of E. coli is carefully matched to the demand for protein synthesis posed by a given growth condition. For example, the fraction of RNA polymerases that transcribe rRNA and tRNA drops from 80% during rapid growth to 24% within minutes of a sudden amino acid starvation. We recently reported in Nucleic Acids Research that the tRNA pool is more dynamically regulated than previously thought. In addition to the regulation at the level of synthesis, we found that tRNAs are subject to demand-based regulation at the level of their degradation. In this point-of-view article we address the question of why this phenomenon has not previously been described. We also present data that expands on the mechanism of tRNA degradation, and we discuss the possible implications of tRNA instability for the ability of E. coli to cope with stresses that affect the translation process.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Transfer RNA instability as a stress response inEscherichia coli: Rapid dynamics of the tRNA pool as a function of demand

2018

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“…However, the remainder of these codons are read by tRNAs that occur at higher levels. For example, Ala1B decoding GCA, GCU, and GCG, Gly3 decoding GGC (along with GGU), Gly2 decoding GGA (along with GGG), Asp1 decoding GAU and GAC, Val1 decoding GUA (along with GUG and GUU), and Ile1 decoding AUU (along with AUC) occur at 5.96, 6.76, 3.31, 3.72, 5.96, and 5.39% of the levels of the total cellular tRNA, respectively (7).…”

Section: Resultsmentioning

confidence: 99%

“…In addition, although UGU and UGC codons for Cys, ACU and ACG codons for Thr, or CAC and CAU codons for His are less frequently used, they are not defined as rare codons (4). Furthermore, it has been shown that the levels of charged tRNA determine if a particular codon would be translated efficiently; and the concentration of tRNA isoacceptors is often positively correlated with the frequency of the occurrence of the cognate codon(s) they read (7,15).…”

Section: Discussionmentioning

confidence: 99%

Functional Significance of an Evolutionarily Conserved Alanine (GCA) Resume Codon in tmRNA in Escherichia coli

Kapoor¹,

Samhita²,

Varshney³

2011

Journal of Bacteriology

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Occasionally, ribosomes stall on mRNAs prior to the completion of the polypeptide chain. In Escherichia coli and other eubacteria, tmRNA-mediated trans-translation is a major mechanism that recycles the stalled ribosomes. The tmRNA possesses a tRNA-like domain and a short mRNA region encoding a short peptide (ANDENYALAA in E. coli) followed by a termination codon. The first amino acid (Ala) of this peptide encoded by the resume codon (GCN) is highly conserved in tmRNAs in different species. However, reasons for the high evolutionary conservation of the resume codon identity have remained unclear. In this study, we show that changing the E. coli tmRNA resume codon to other efficiently translatable codons retains efficient functioning of the tmRNA. However, when the resume codon was replaced with the low-usage codons, its function was adversely affected. Interestingly, expression of tRNAs decoding the low-usage codon from plasmid-borne gene copies restored efficient utilization of tmRNA. We discuss why in E. coli, the GCA (Ala) is one of the best codons and why all codons in the short mRNA of the tmRNA are decoded by the abundant tRNAs.Occasionally, during the process of translation, ribosomes stall on mRNAs prior to the completion of the polypeptide chain. If not recycled, accumulation of the stalled ribosomes is detrimental to the organism as it sequesters not only the ribosomes but also the tRNAs (as peptidyl-tRNAs) and brings protein synthesis to a halt. In Escherichia coli and other eubacteria, a well-known pathway that recycles the stalled ribosomes utilizes tmRNA (SsrA or 10Sa RNA) by a process called trans-translation (18,36). The tmRNA contains a tRNA like domain and an mRNA region encoding a short peptide (AN DENYALAA in E. coli) followed by a termination codon (Fig. 1A). The tmRNA is aminoacylated with alanine (in its tRNAlike domain) and recruited to the A-site of the ribosome stalled on a truncated mRNA. The polypeptide from the P-site tRNA is transferred to the alanine on the tRNA-like domain of tm-RNA to form (peptidyl)-alanyl-tmRNA. The ribosome then resumes translation (trans-translation) decoding the first codon (the "resume codon") and the remaining codons of the short open reading frame in the tmRNA. When the termination codon in the tmRNA reaches the ribosomal A-site, the C-terminally tagged polypeptide is released. Thus, the process of trans-translation in E. coli appends AANDENYALAA sequence to the incomplete polypeptide and marks it for degradation by cellular proteases. The C-terminal amino acids in the appended sequence are important for recognition by the cellular proteases; and while the tmRNA mutants that encode ANDENYALDD or ANDEHHHHHH rescue the stalled ribosomes, they do not direct the tagged proteins to degradation (9,11,17,25). Interestingly, the first amino acid (Ala) of the short peptide encoded by the resume codon GCN is evolutionarily conserved across the tmRNA sequences from different species. In addition, although the ssrA mutants harboring alternate resume codons have been...

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“…The PURE system contains 9 translation factors, 20 aa-tRNA synthetases (aaRSs), 6 additional enzymes (also needed for energy regeneration), ribosomes, tRNAs, and low molecular weight compounds. There are 36 different purified macromolecular compounds, and presumably 46 different tRNAs (Dong et al, 1996), for a total of 82 different macromolecules. If we sum the template DNA it results that 83 different compounds are involved in coupled transcription/translation reactions (prokaryote ribosomes consists in 3 rRNAs and 55 ribosomal proteins, and therefore the overall number of different macromolecular sequences in the PURE system actually sums up to 141).…”

Section: The Technology For Building Minimal Cellsmentioning

confidence: 99%

Advances in Minimal Cell Models: a New Approach to Synthetic Biology and Origin of Life

Stano¹

2011

Progress in Molecular and Environmental Bioengineering - From Analysis and Modeling to Technology Applications

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Co-variation of tRNA Abundance and Codon Usage inEscherichia coliat Different Growth Rates

Cited by 756 publications

References 20 publications

Transfer RNA instability as a stress response inEscherichia coli: Rapid dynamics of the tRNA pool as a function of demand

Transfer RNA instability as a stress response inEscherichia coli: Rapid dynamics of the tRNA pool as a function of demand

Functional Significance of an Evolutionarily Conserved Alanine (GCA) Resume Codon in tmRNA in Escherichia coli

Advances in Minimal Cell Models: a New Approach to Synthetic Biology and Origin of Life

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