Deletion of the ribosomal protein gene rpmJ activates zntA transcription through a translation-dependent mechanism in Escherichia coli

Bacteria tightly regulate intracellular zinc homeostasis by coordinating zinc uptake and efflux systems. We previously showed that deletion of the ribosomal protein gene rpmJ confers zinc resistance in Escherichia coli in a manner dependent on the zinc efflux transporter zntA. Here, we analyzed the effect of rpmJ deficiency on zntA expression. Under zinc excess conditions, zntA mRNA levels were markedly higher in the rpmJ mutant than in the wild-type strain. Enhanced zntA expression required the native zntA promoter, the native Shine-Dalgarno sequence, and the N-terminal coding region of zntA, indicating that translation initiated from the native Shine-Dalgarno sequence and extending through the N-terminal coding region is required for enhanced transcription initiation from the native zntA promoter. Furthermore, ectopic expression of ykgO, a paralog of rpmJ that is known to replace RpmJ on the ribosome under zinc-limited conditions, abolished the increased zntA expression and zinc resistance conferred by rpmJ deletion. Collectively, these findings suggest that ribosomes lacking RpmJ or YkgO promote transcription initiation from the native zntA promoter through translation of zntA mRNA. IMPORTANCEBacteria must carefully control the amount of zinc inside their cells. Too little zinc prevents essential cellular processes, whereas too much zinc is toxic. We found that removing a small ribosomal protein called RpmJ allows Escherichia coli to survive high zinc levels by increasing production of the zinc exporter zntA. Surprisingly, this increase depends not only on the zntA promoter but also on translation of the beginning of the zntA coding region. Our findings suggest that changes in ribosome composition can stimulate gene transcription through early translation of the same messenger RNA, revealing a previously unrecognized mechanism linking translation and transcription during bacterial adaptation to zinc stress.