Indole cell signaling occurs primarily at low temperatures in Escherichia coli

Jintae Lee, Xue Song Zhang, Manjunath Hegde, William E. Bentley, Arul Jayaraman, Thomas Keith Wood

Research output: Contribution to journalArticle

77 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)1007-1023
Number of pages17
JournalISME Journal
Volume2
Issue number10
DOIs
StatePublished - Oct 1 2008

Fingerprint

indoles
Escherichia coli
Temperature
gene
temperature
Genes
cells
uridine monophosphate
genes
Biofilms
biofilm
Uridine Monophosphate
Quorum Sensing
uracil
quorum sensing
Uracil
gene expression
Enterohemorrhagic Escherichia coli
Gene Expression
antibiotic resistance

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Lee, Jintae ; Zhang, Xue Song ; Hegde, Manjunath ; Bentley, William E. ; Jayaraman, Arul ; Wood, Thomas Keith. / Indole cell signaling occurs primarily at low temperatures in Escherichia coli. In: ISME Journal. 2008 ; Vol. 2, No. 10. pp. 1007-1023.
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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.",
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Lee, J, Zhang, XS, Hegde, M, Bentley, WE, Jayaraman, A & Wood, TK 2008, 'Indole cell signaling occurs primarily at low temperatures in Escherichia coli', ISME Journal, vol. 2, no. 10, pp. 1007-1023. https://doi.org/10.1038/ismej.2008.54

Indole cell signaling occurs primarily at low temperatures in Escherichia coli. / Lee, Jintae; Zhang, Xue Song; Hegde, Manjunath; Bentley, William E.; Jayaraman, Arul; Wood, Thomas Keith.

In: ISME Journal, Vol. 2, No. 10, 01.10.2008, p. 1007-1023.

Research output: Contribution to journalArticle

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AU - Lee, Jintae

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