Abstract
In fast-growing microorganisms, a tRNA concentration profile enriched in major isoacceptors selects for the biased usage of cognate codons. This optimizes translational rate for the least mass invested in the translational apparatus. Such translational streamlining is thought to be growth-regulated, but its genetic basis is poorly understood. First, we found in reanalysis of the E. coli tRNA profile that the degree to which it is translationally streamlined is nearly invariant with growth rate. Then, using least squares multiple regression, we partitioned tRNA isoacceptor pools to predicted tDNA operons from the E. coli K12 genome. Co-expression of tDNAs in operons explains the tRNA profile significantly better than tDNA gene dosage alone. Also, operon expression increases significantly with proximity to the origin of replication, oriC, at all growth rates. Genome location explains about 15% of expression variation in a form, at a given growth rate, that is consistent with replication-dependent gene concentration effects. Yet the change in the tRNA profile with growth rate is less than would be expected from such effects. We estimated per-copy expression rates for all tDNA operons that were consistent with independent estimates for rDNA operons. We also found that tDNA operon location, and the location dependence of expression, were significantly different in the leading and lagging strands. The operonic organization and genomic location of tDNA operons are significant factors influencing their expression. Nonrandom patterns of location and strandedness shown by tDNA operons in E. coli suggest that their genomic architecture may be under selection to satisfy physiological demand for tRNA expression at high growth rates.
Highlights
During balanced growth in rich media, prokaryotic and eukaryotic microorganisms selected to grow efficiently are enriched in ‘‘major’’ isoacceptor tRNAs cognate to ‘‘preferred’’ codons in the transcriptome [1,2]
We show that a large fraction of the variation in tDNA operon expression must be explained by localized differences in regulatory elements and precursor structure, a significant fraction of variation in the E. coli tRNA profile is explained by the genomic location of tDNA operons
We conclude that the operon model explains tRNA concentration data significantly better than gene dosage alone
Summary
During balanced growth in rich media, prokaryotic and eukaryotic microorganisms selected to grow efficiently are enriched in ‘‘major’’ isoacceptor tRNAs cognate to ‘‘preferred’’ codons in the transcriptome [1,2]. Its authors find that concentrations of major isoacceptors increase with growth rate but only about 2-fold, from l 1⁄4 0.4 to l 1⁄4 2.5 doublings/h, less than had been found in the previous studies, while minor isoacceptor concentrations remained approximately the same They conclude that the data are consistent with the hypothesis of growth-rate-dependent enrichment of the tRNA profile, a hypothesis that we call growth-regulated translational streamlining. There is some evidence for replication-dependent effects on tDNA operon expression, this cannot explain how constant the tRNA profile is with growth rate. Transposition of certain reporter genes toward the origin of replication increases their total relative expression at a specific growth rate in a manner fully consistent with theory [14,16] In light of these results, we wanted to ask whether replication-dependent effects of genomic location on operon concentration (position effects) can explain the biased tRNA profile in E. coli. Growth regulation of the tRNA profile may be inessential to the theory that E. coli achieves a growth advantage through translational streamlining
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