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The genetic code underlying protein synthesis is a canonical example of adegenerate biological system. Degeneracies in physical and biological systemscan be lifted by external perturbations thus allowing degenerate systems toexhibit a wide range of behaviors. Here we show that the degeneracy of thegenetic code is lifted by environmental perturbations to regulate proteinlevels in living cells. By measuring protein synthesis rates from a syntheticreporter library in Escherichia coli, we find that environmental perturbations,such as reduction of cognate amino acid supply, lift the degeneracy of thegenetic code by splitting codon families into a hierarchy of robust andsensitive synonymous codons. Rates of protein synthesis associated with robustcodons are up to hundred-fold higher than those associated with sensitivecodons under these conditions. We find that the observed hierarchy betweensynonymous codons is not determined by usual rules associated with tRNAabundance and codon usage. Rather, competition among tRNA isoacceptors foraminoacylation underlies the robustness of protein synthesis. Remarkably, thehierarchy established using the synthetic library also explains the measuredrobustness of synthesis for endogenous proteins in E. coli. We further foundthat the same hierarchy is reflected in the fitness cost of synonymousmutations in amino acid biosynthesis genes and in the transcriptional controlof sigma factor genes. Our study reveals that the degeneracy of the geneticcode can be lifted by environmental perturbations, and it suggests thatorganisms can exploit degeneracy lifting as a general strategy to adapt proteinsynthesis to their environment.

Environmental perturbations lift the degeneracy of the genetic code to regulate protein levels in bacteria