16S ribosomal RNA modification drives transcript-specific translation efficiency

Bacterial ribosomal RNAs (rRNAs) are decorated with conserved nucleotide modifications, but the functionality of these modifications is often underexplored. MraW (RsmH) is a 16S rRNA methyltransferase. Here, we report that deletion of mraW corrects a late-stage sporulation defect in Bacillus subtilis by bypassing a sporulation checkpoint. Ribosomes purified from ΔmraW cells display a ∼2-fold decrease in translation efficiency; in vivo, ΔmraW cells produced decreased levels of the sporulation checkpoint protein CmpA. Reduced production of CmpA is mediated by mRNA sequences that form a stem-loop which occludes early cmpA codons. Proteomic analysis revealed that MraW mediates production of multiple proteins, some of whose mRNA form similar structures as the cmpA transcript. We propose that MraW modification of 16S rRNA enhances translation efficiency in general, and that specific transcripts have evolved structural features that fine-tune protein levels. This type of control may be prevalent in bacteria which exhibit uncoupled transcription and translation.