Indole cell signaling occurs primarily at low temperatures in Escherichia coli.
We have shown that the quorum-sensing signals acylhomoserine lactones, autoinducer-2 (AI-2) and indole influence the biofilm formation of Escherichia coli. Here, we investigate how the environment, that is, temperature, affects indole and AI-2 signaling in E. coli. We show in biofilms that indole addition leads to more extensive differential gene expression at 30 degrees C (186 genes) than at 37 degrees C (59 genes), that indole reduces biofilm formation (without affecting growth) more significantly at 25 and 30 degrees C than at 37 degrees C and that the effect is associated with the quorum-sensing protein SdiA. The addition of indole at 30 degrees C compared to 37 degrees C most significantly repressed genes involved in uridine monophosphate (UMP) biosynthesis (carAB, pyrLBI, pyrC, pyrD, pyrF and upp) and uracil transport (uraA). These uracil-related genes are also repressed at 30 degrees C by SdiA, which confirms SdiA is involved in indole signaling. Also, compared to 37 degrees C, indole more significantly decreased flagella-related qseB, flhD and fliA promoter activity, enhanced antibiotic resistance and inhibited cell division at 30 degrees C. In contrast to indole and SdiA, the addition of (S)-4,5-dihydroxy-2,3-pentanedione (the AI-2 precursor) leads to more extensive differential gene expression at 37 degrees C (63 genes) than at 30 degrees C (11 genes), and, rather than repressing UMP synthesis genes, AI-2 induces them at 37 degrees C (but not at 30 degrees C). Also, the addition of AI-2 induces the transcription of virulence genes in enterohemorrhagic E. coli O157:H7 at 37 degrees C but not at 30 degrees C. Hence, cell signals cause diverse responses at different temperatures, and indole- and AI-2-based signaling are intertwined.
Lee
Jintae
J
Artie McFerrin Department of Chemical Engineering, Texas A & M University, College Station, TX 77843-3122, USA.
Zhang
Xue-Song
XS
Hegde
Manjunath
M
Bentley
William E
WE
Jayaraman
Arul
A
Wood
Thomas K
TK
D018441:Biofilms / Q000254:growth & development; D002455:Cell Division; D024881:Drug Resistance, Bacterial; D004926:Escherichia coli / Q000187:drug effects / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D029968:Escherichia coli Proteins / Q000235:genetics / Q000378:metabolism; D005407:Flagella / Q000235:genetics / Q000378:metabolism; D015964:Gene Expression Regulation, Bacterial; D006714:Homoserine / Q000031:analogs & derivatives / Q000378:metabolism; D007211:Indoles / Q000378:metabolism*; D007783:Lactones / Q000378:metabolism; D008969:Molecular Sequence Data; D015398:Signal Transduction; D013696:Temperature; D015534:Trans-Activators / Q000235:genetics / Q000378:metabolism
D029968:Escherichia coli Proteins; D007211:Indoles; D007783:Lactones; C091088:N-octanoylhomoserine lactone; D015534:Trans-Activators; C490806:sdiA protein, E coli; D006714:Homoserine; C030374:indole