Promoter-proximal transcription-translation coupling controls early transcription in Escherichia coli

The functional coupling of transcription and translation contributes significantly to maintaining messenger RNA (mRNA) expression in bacterial cells. Premature transcription termination and fast mRNA decay are known to limit the expression of mRNAs when transcription is decoupled from translation. Here, we report that inhibiting the generation of untranslatable mRNAs from the promoter-proximal region is a newly identified but essential pathway of mRNA quality control by transcription-translation decoupling. The promoter-proximal region of mRNAs, the amount of which reflects early transcription in the 5'-untranslated region, is not generated without translation. The decoupling between transcription and translation results in RNA polymerase (RNAP) traffic within 250 bp from the transcription start site, hindering productive early transcription. The limited processivity of RNAP without a coupled ribosome in the promoter-proximal region is further supported by the observation that decoupled RNAP elongates mRNA by only 80-90 bp on average in vivo. Our results demonstrate that ribosome coupling near the promoter-proximal region is critical for the efficient synthesis of translatable mRNAs by RNAPs.