A highly conserved sRNA downregulates multiple genes, including a σ transcriptional activator, in the virulence mode of .

Bacterial sRNAs together with the RNA chaperone Hfq post-transcriptionally regulate gene expression by affecting ribosome binding or mRNA stability. In the human pathogen , the causative agent of whooping cough, hundreds of sRNAs have been identified, but their roles in biology are mostly unknown. Here we characterize a Hfq-dependent sRNA (S17), whose level is dramatically higher in the virulence (Bvg) mode. We show that transcription from a σ-dependent promoter yields a long form of 190 nucleotides (nts) that is processed by RNase E to generate a shorter, more stable form (S17S) of 67 nts. Using RNA-seq and RT-qPCR, we identify 92 genes whose expression significantly increases in the absence of S17. Of these genes, 70 contain sequences at/near their ribosome binding sites (RBSs) that are complementary to single-stranded (ss) regions (Sites 1 or 2) of S17S. The identified genes include those encoding multiple transporters and 3 transcriptional regulators. Using a translational reporter system, we demonstrate that S17S directly represses one of these genes, , a σ-dependent transcriptional regulator, suggesting the repression of a σ regulon in the Bvg mode. We find that the S17S region containing Sites 1 and 2 is 100% conserved throughout various Betaproteobacteria species, and the S17S target sites are often conserved in the homologs of the target genes. We speculate that S17S regulation represents a highly conserved process that fine-tunes gene expression in the Bvg mode of and perhaps under other conditions in related bacteria.