The second messenger cyclic diguanylic acid (c-di-GMP) is implicated in key lifestyle decisions of bacteria, including biofilm formation and changes in motility and virulence. Some challenges in deciphering the physiological roles of c-di-GMP are the limited knowledge about the cellular targets of c-di-GMP, the signals that control its levels, and the proportion of free cellular c-di-GMP, if any. Here, we identify the target and the regulatory signal for a c-di-GMP-responsive Escherichia coli ribonucleoprotein complex. We show that a direct c-di-GMP target in E. coli is polynucleotide phosphorylase (PNPase), an important enzyme in RNA metabolism that serves as a 3' polyribonucleotide polymerase or a 3'-to-5' exoribonuclease. We further show that a complex of polynucleotide phosphorylase with the direct oxygen sensors DosC and DosP can perform oxygen-dependent RNA processing. We conclude that c-di-GMP can mediate signal-dependent RNA processing and that macromolecular complexes can compartmentalize c-di-GMP signaling.
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