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In bacteria, RNA-binding proteins of the RsmA/CsrA family act as post-transcriptional regulators that modulate translation initiation at target transcripts. The  Pseudomonas aeruginosa  genome contains two phenazine biosynthetic ( phz ) gene clusters,  phzA1-G1  ( phz1 ) and  phzA2-G2  ( phz2 ), each of which is responsible for phenazine-1-carboxylic acid (PCA) biosynthesis. In the present study, we show that RsmA exhibits differential gene regulation on two  phz  clusters in  P. aeruginosa  M18 at the post-transcriptional level. Based on the sequence analysis, four GGA motifs, the potential RsmA binding sites, are found on the 5′-untranslated region (UTR) of the  phz2  transcript. Studies with a series of  lacZ  reporter fusions, and gel mobility shift assays suggest that the third GGA motif (S3), located 21 nucleotides upstream of the Shine-Dalgarno (SD) sequence, is involved in direct RsmA-mediated activation of  phz2  expression. We therefore propose a novel model in which the binding of RsmA to the target S3 results in the destabilization of the stem-loop structure and the enhancement of ribosome access. This model could be fully supported by RNA structure prediction, free energy calculations, and nucleotide replacement studies. In contrast, various RsmA-mediated translation repression mechanisms have been identified in which RsmA binds near the SD sequence of target transcripts, thereby blocking ribosome access. Similarly, RsmA is shown to negatively regulate  phz1  expression. Our new findings suggest that the differential regulation exerted by RsmA on the two  phz  clusters may confer an advantage to  P. aeruginosa  over other pseudomonads containing only a single  phz  cluster in their genomes.

The phzA2-G2 Transcript Exhibits Direct RsmA-Mediated Activation in Pseudomonas aeruginosa M18