The Transcription Regulator and c-di-GMP Phosphodiesterase PdeL Represses Motility in Escherichia coli

ABSTRACT

PdeL is a transcription regulator and catalytically active c-di-GMP phosphodiesterase (PDE) in Escherichia coli. PdeL has been shown to be a transcription autoregulator, while no other target genes have been identified so far. Here, we show that PdeL represses the transcription of the flagellar class II operon fliFGHIJK and activates sslE, encoding an extracellularly anchored metalloprotease, among additional loci. DNA-binding studies and expression analyses using plasmidic reporters suggest that the regulation of the fliF and sslE promoters by PdeL is direct. Transcription repression of the fliFGHIJK operon, encoding proteins required for the assembly of the flagellar basal body, results in inhibition of motility on soft-agar plates and reduction of flagellum assembly, as shown by fluorescence staining of the flagellar hook protein FlgE. PdeL-mediated repression of motility is independent of its phosphodiesterase activity. Thus, in motility control, the transcription regulator function of PdeL in reducing the number of assembled flagella is apparently epistatic to its phosphodiesterase function, which can indirectly promote the activity of the flagellar motor by lowering the c-di-GMP concentration.

IMPORTANCE Bacteria adopt different lifestyles depending on their environment and physiological conditions. In Escherichia coli and other enteric bacteria, the transition between the motile and the sessile states is controlled at multiple levels from the regulation of gene expression to the modulation of various processes by the second messenger c-di-GMP as a signaling molecule. The significance of our research is in identifying PdeL, a protein of dual function that hydrolyzes c-di-GMP and regulates the transcription of genes, as a repressor of flagellar gene expression and an inhibitor of motility, which adds an additional regulatory switch to the control of motility.