Selective recruitment of stress-responsive mRNAs to ribosomes for translation by acetylated protein S1 during nutrient stress in Escherichia coli.

The chemical modification of ribosomes plays an important regulatory role in cellular translation adaptation in response to environmental stresses. Nevertheless, how the modified ribosome reprograms the translation machinery for the preferential expression of the specific mRNAs encoding stress-responsive proteins to stress remains poorly understood. Here, we find that AcP-induced acetylation of K411 and K464 in ribosomal protein S1 during carbon-nitrogen imbalance, which in turn impacts its binding with distinct mRNAs. S1 acetylation shows differential selectivity for recruiting subsets of mRNAs to ribosomes. Using the RNC-Seq method, we find that mimic acetylated S1 prefers transcripts related with the formation of flagella/biofilms, two-component systems, nitrogen assimilation, amino acid degradation, and lipopolysaccharide biosynthesis, whereas inhibits the translation of mRNAs involved in amino acid biosynthesis and most ribosomal proteins. Importantly, further characterization of S1-binding site (SBS) sequences of mRNAs with different translation efficiencies indicated that the presence of a conserved motif allows coordinated regulation of S1 acetylation-driven translation reprogramming for cell survival during nitrogen starvation. These findings expand the repertoire of ribosome heterogeneity to the acetylation level of S1 at specific sites and its role in the ribosome-mediated regulation of gene expression as a cellular response at the translational level to stress.