Cyclic-di-GMP-mediated signalling within the sigma network of Escherichia coli.
Bis-(3'-5')-cyclic-di-guanosine monophosphate (c-di-GMP) is a bacterial signalling molecule produced by diguanylate cyclases (DGC, carrying GGDEF domains) and degraded by specific phosphodiesterases (PDE, carrying EAL domains). Neither its full physiological impact nor its effector mechanisms are currently understood. Also, the existence of multiple GGDEF/EAL genes in the genomes of most species raises questions about output specificity and robustness of c-di-GMP signalling. Using microarray and gene fusion analyses, we demonstrate that at least five of the 29 GGDEF/EAL genes in Escherichia coli are not only stationary phase-induced under the control of the general stress response master regulator sigma(S) (RpoS), but also exhibit differential control by additional environmental and temporal signals. Two of the corresponding proteins, YdaM (GGDEF only) and YciR (GGDEF + EAL), which in vitro show DGC and PDE activity, respectively, play an antagonistic role in the expression of the biofilm-associated curli fimbriae. This control occurs at the level of transcription of the curli and cellulose regulator CsgD. Moreover, we show that H-NS positively affects curli expression by inversely controlling the expression of ydaM and yciR. Furthermore, we demonstrate a temporally fine-tuned GGDEF cascade in which YdaM controls the expression of another GGDEF protein, YaiC. By genome-wide microarray analysis, evidence is provided that YdaM and YciR strongly and nearly exclusively control CsgD-regulated genes. We conclude that specific GGDEF/EAL proteins have very distinct expression patterns, and when present in physiological amounts, can act in a highly precise, non-global and perhaps microcompartmented manner on a few or even a single specific target(s).
Weber
Harald
H
Institut für Biologie, Mikrobiologie, Freie Universität Berlin, 14195 Berlin, Germany.
Pesavento
Christina
C
Possling
Alexandra
A
Tischendorf
Gilbert
G
Hengge
Regine
R
D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D018441:Biofilms; D006152:Cyclic GMP / Q000031:analogs & derivatives* / Q000378:metabolism; D004926:Escherichia coli / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D029968:Escherichia coli Proteins / Q000235:genetics / Q000502:physiology; D010861:Fimbriae, Bacterial / Q000235:genetics / Q000648:ultrastructure; D015964:Gene Expression Regulation, Bacterial; D020411:Oligonucleotide Array Sequence Analysis; D010641:Phenotype; D019761:Phosphorus-Oxygen Lyases / Q000502:physiology; D017434:Protein Structure, Tertiary; D012808:Sigma Factor / Q000235:genetics / Q000378:metabolism*; D015398:Signal Transduction; D015534:Trans-Activators / Q000235:genetics
D001426:Bacterial Proteins; C499694:CsgD protein, E coli; D029968:Escherichia coli Proteins; C430113:Gmr protein, E coli; D012808:Sigma Factor; D015534:Trans-Activators; C069567:sigma factor KatF protein, Bacteria; C077481:Crl protein, Bacteria; C062025:bis(3',5')-cyclic diguanylic acid; D019761:Phosphorus-Oxygen Lyases; C517137:YdaM protein, E coli; D006152:Cyclic GMP