Carbon Catabolite repression (CCR) allows a fast adaptation of Bacteria to changing nutrient supplies. The Pseudomonas aeruginosa (PAO1) catabolite repression control protein (Crc) was deemed to act as a translational regulator, repressing functions involved in uptake and utilization of carbon sources. However, Crc of PAO1 was recently shown to be devoid of RNA binding activity. In this study the RNA chaperone Hfq was identified as the principle post-transcriptional regulator of CCR in PAO1. Hfq is shown to bind to A-rich sequences within the ribosome binding site of the model mRNA amiE, and to repress translation in vitro and in vivo. We further report that Crc plays an unknown ancillary role, as full-fledged repression of amiE and other CCR-regulated mRNAs in vivo required its presence. Moreover, we show that the regulatory RNA CrcZ, transcription of which is augmented when CCR is alleviated, binds to Hfq with high affinity. This study on CCR in PAO1 revealed a novel concept for Hfq function, wherein the regulatory RNA CrcZ acts as a decoy to abrogate Hfq-mediated translational repression of catabolic genes and thus highlights the central role of RNA based regulation in CCR of PAO1.
Carbon assimilation in Bacteria is governed by a mechanism known as carbon catabolite repression (CCR). In contrast to several other bacterial clades CCR in Pseudomonas species appears to be primarily regulated at the post-transcriptional level. In this study, we have identified the RNA chaperone Hfq as the principle post-transcriptional regulator of CCR in P. aeruginosa (PAO1). Hfq is shown to act as a translational regulator and to prevent ribosome loading through binding to A-rich sequences within the ribosome binding site of mRNAs, which encode enzymes involved in carbon utilization. It has been previously shown that the synthesis of the RNA CrcZ is augmented in the presence of non-preferred carbon sources. Here, we show that the CrcZ RNA binds to and sequesters Hfq, which in turn abrogates Hfq-mediated translational repression of mRNAs, the encoded functions of which are required for the breakdown of non-preferred carbon sources. This novel mechanistic twist on Hfq function not only highlights the central role of RNA based regulation in CCR of PAO1 but also broadens the view of Hfq-mediated post-transcriptional mechanisms.
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