The Bacterial Transcription Termination Factor Rho Coordinates Mg2+ Homeostasis with Translational Signals

Abstract

The bacterial protein Rho triggers transcription termination at the ends of many operons and when transcription and translation become uncoupled. In addition to these genome-wide activities, Rho implements regulation of specific genes by dictating whether RNA polymerase terminates transcription within the 5’ leader region or continues into the downstream coding region. Here, we report that the Mg2+ channel gene corA in Salmonella enterica serovar Typhimurium, which was previously thought to be constitutively expressed, is regulated by a Rho-dependent terminator located within its 5’ leader region. We demonstrate that the unusually long and highly conserved corA leader mRNA can adopt two mutually exclusive conformations that determine whether or not Rho interacts with a Rho utilization (rut) site on the nascent RNA and thereby prevents transcription of the corA coding region. The RNA conformation that promotes Rho-dependent termination is favored by efficient translation of corL, a short open reading frame located within the corA leader. Thus, corA transcription is inversely coupled to corL translation. This mechanism resembles those governing expression of Salmonella’s other two Mg2+ transport genes, suggesting that Rho links Mg2+ uptake to translational signals.

Transcription termination factor Rho: a hub linking diverse physiological processes in bacteria

“…Expression of the Mg 2+ channel gene corA was shown to be regulated by a Rho-dependent terminator located within its 59 leader region. Accessibility of the rut site depending on RNA conformation was shown to be modulated by translation of corL, a short orf located within the corA gene (Kriner & Groisman, 2015).…”

“…A new Rho-dependent mechanism was described for expression of Salmonella genes involved in Mg 2+ transport, suggesting that Rho links Mg 2+ uptake to translational signals (Kriner & Groisman, 2015). Expression of the Mg 2+ channel gene corA was shown to be regulated by a Rho-dependent terminator located within its 59 leader region.…”

“…In E. coli, the 109 nt long Spot 42 sRNA encoded by the spf gene is known to downregulate expression of galK, the third gene of the galactose operon galETKM, thereby inhibiting GalK production (Møller et al, 2002). Recent studies suggested that Spot 42 regulates galK expression at two levels: RNA degradation and enhancement of Rho-dependent transcription termination at the A new Rho-dependent mechanism was described for expression of Salmonella genes involved in Mg 2+ transport, suggesting that Rho links Mg 2+ uptake to translational signals (Kriner & Groisman, 2015). Expression of the Mg 2+ channel gene corA was shown to be regulated by a Rho-dependent terminator located within its 59 leader region.…”

“…Expression of the Mg 2+ channel gene corA was shown to be regulated by a Rho-dependent terminator located within its 59 leader region. Accessibility of the rut site depending on RNA conformation was shown to be modulated by translation of corL, a short orf located within the corA gene (Kriner & Groisman, 2015).Another example of gene regulation implicating Rho is the regulation of the E. coli pgaABCD operon by the CsrA protein (Figueroa-Bossi et al, 2014). The 59 UTR of the pgaABCD operon was shown to contain a rut site which is sequestered by stable RNA secondary structure.…”

Learning from the Leaders: Gene Regulation by the Transcription Termination Factor Rho

“…Unlike their constitutive counterparts, the efficiency of regulated Rho-dependent terminators is controlled by cytoplasmic signal(s) sensed by a variety of factors [8, 43, 58, 59]. In the case of the otherwise constitutive tR1 terminator located within the major rightward operon of bacteriophage λ, Rho-dependent termination is abolished by binding of the phage N protein to an RNA hairpin located within the rut site [60, 61].…”