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

<jats:title>ABSTRACT</jats:title> <jats:p> Bacteria tightly regulate intracellular zinc homeostasis by coordinating zinc uptake and efflux systems. We previously showed that deletion of the ribosomal protein gene <jats:italic>rpmJ</jats:italic> confers zinc resistance in <jats:italic>Escherichia coli</jats:italic> in a manner dependent on the zinc efflux transporter <jats:italic>zntA</jats:italic> . Here, we analyzed the effect of <jats:italic>rpmJ</jats:italic> deficiency on <jats:italic>zntA</jats:italic> expression. Under zinc excess conditions, <jats:italic>zntA</jats:italic> mRNA levels were markedly higher in the <jats:italic>rpmJ</jats:italic> mutant than in the wild-type strain. Enhanced <jats:italic>zntA</jats:italic> expression required the native <jats:italic>zntA</jats:italic> promoter, the native Shine–Dalgarno sequence, and the N-terminal coding region of <jats:italic>zntA</jats:italic> , 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 <jats:italic>zntA</jats:italic> promoter. Furthermore, ectopic expression of <jats:italic>ykgO</jats:italic> , a paralog of <jats:italic>rpmJ</jats:italic> that is known to replace RpmJ on the ribosome under zinc-limited conditions, abolished the increased <jats:italic>zntA</jats:italic> expression and zinc resistance conferred by <jats:italic>rpmJ</jats:italic> deletion. Collectively, these findings suggest that ribosomes lacking RpmJ or YkgO promote transcription initiation from the native <jats:italic>zntA</jats:italic> promoter through translation of <jats:italic>zntA</jats:italic> mRNA. </jats:p> <jats:sec> <jats:title>IMPORTANCE</jats:title> <jats:p> Bacteria 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 <jats:italic>Escherichia coli</jats:italic> to survive high zinc levels by increasing production of the zinc exporter <jats:italic>zntA</jats:italic> . Surprisingly, this increase depends not only on the <jats:italic>zntA</jats:italic> promoter but also on translation of the beginning of the <jats:italic>zntA</jats:italic> 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. </jats:p> </jats:sec>