1. ¹Artie McFerrin Department of Chemical Engineering, Texas A & M University, College Station, TX, USA
2. ²Fischell Department of Bioengineering, University of Maryland, College Park, MD, USA
3. ³The Department of Biology, Texas A & M University, College Station, TX, USA
4. ⁴The Zachry Department of Civil Engineering, Texas A & M University, College Station, TX, USA

Correspondence: TK Wood, Chemical Engineering, Texas A & M University, 220 J.E. Brown Building, 3122 TAMU, College Station, TX 77843-3122, USA. E-mail: thomas.wood@chemail.tamu.edu

Received 18 February 2008; Revised 13 May 2008; Accepted 13 May 2008; Published online 5 June 2008.

Abstract

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 °C (186 genes) than at 37 °C (59 genes), that indole reduces biofilm formation (without affecting growth) more significantly at 25 and 30 °C than at 37 °C and that the effect is associated with the quorum-sensing protein SdiA. The addition of indole at 30 °C compared to 37 °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 °C by SdiA, which confirms SdiA is involved in indole signaling. Also, compared to 37 °C, indole more significantly decreased flagella-related qseB, flhD and fliA promoter activity, enhanced antibiotic resistance and inhibited cell division at 30 °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 °C (63 genes) than at 30 °C (11 genes), and, rather than repressing UMP synthesis genes, AI-2 induces them at 37 °C (but not at 30 °C). Also, the addition of AI-2 induces the transcription of virulence genes in enterohemorrhagic E. coli O157:H7 at 37 °C but not at 30 °C. Hence, cell signals cause diverse responses at different temperatures, and indole- and AI-2-based signaling are intertwined.