An RNA sponge directs the transition from feast to famine in Caulobacter crescentus

In bacteria, regulatory networks controlling the adaptation of gene expression in response to stress are frequently complemented by base-pairing small regulatory RNAs (sRNAs) that act at the post-transcriptional level. While many regulatory circuits governing stress resilience have been studied in the model bacterium Caulobacter crescentus, only a small fraction of its diverse sRNA repertoire has been characterized. In this study, we globally identified interacting RNA-RNA pairs associated with the major RNA-binding protein Hfq in C. crescentus. In addition to numerous connections between sRNAs and mRNAs, we isolated unconventional pairs consisting of two non-coding sRNAs. Our results indicate that the sRNA CrfA acts as a sponge to inactivate a family of four conserved sRNAs, SisA-D. When induced by carbon starvation, CrfA redirects gene expression towards the utilization of distinct energy sources, and loss of the RNA sponge is linked to a severe growth defect in environments with fluctuating nutrient availability.