Indole is an inter-species biofilm signal mediated by SdiA
Open Access
- 18 May 2007
- journal article
- Published by Springer Science and Business Media LLC in BMC Microbiology
- Vol. 7 (1), 42
- https://doi.org/10.1186/1471-2180-7-42
Abstract
As a stationary phase signal, indole is secreted in large quantities into rich medium by Escherichia coli and has been shown to control several genes (e.g., astD, tnaB, gabT), multi-drug exporters, and the pathogenicity island of E. coli; however, its impact on biofilm formation has not been well-studied. Through a series of global transcriptome analyses, confocal microscopy, isogenic mutants, and dual-species biofilms, we show here that indole is a non-toxic signal that controls E. coli biofilms by repressing motility, inducing the sensor of the quorum sensing signal autoinducer-1 (SdiA), and influencing acid resistance (e.g., hdeABD, gadABCEX). Isogenic mutants showed these associated proteins are directly related to biofilm formation (e.g., the sdiA mutation increased biofilm formation 50-fold), and SdiA-mediated transcription was shown to be influenced by indole. The reduction in motility due to indole addition results in the biofilm architecture changing from scattered towers to flat colonies. Additionally, there are 12-fold more E. coli cells in dual-species biofilms grown in the presence of Pseudomonas cells engineered to express toluene o- monooxygenase (TOM, which converts indole to an insoluble indigoid) than in biofilms with pseudomonads that do not express TOM due to a 22-fold reduction in extracellular indole. Also, indole stimulates biofilm formation in pseudomonads. Further evidence that the indole effects are mediated by SdiA and homoserine lactone quorum sensing is that the addition of N-butyryl-, N-hexanoyl-, and N-octanoyl-L-homoserine lactones repress E. coli biofilm formation in the wild-type strain but not with the sdiA mutant. Indole is an interspecies signal that decreases E. coli biofilms through SdiA and increases those of pseudomonads. Indole may be manipulated to control biofilm formation by oxygenases of bacteria that do not synthesize it in a dual-species biofilm. Furthermore, E. coli changes its biofilm in response to signals it cannot synthesize (homoserine lactones), and pseudomonads respond to signals they do not synthesize (indole).Keywords
This publication has 61 references indexed in Scilit:
- Bundle-Forming Pili and EspA Are Involved in Biofilm Formation by EnteropathogenicEscherichia coliJournal of Bacteriology, 2006
- YliH (BssR) and YceP (BssS) Regulate Escherichia coli K-12 Biofilm Formation by Influencing Cell SignalingApplied and Environmental Microbiology, 2006
- Structure of the Escherichia coli Quorum Sensing Protein SdiA: Activation of the Folding Switch by Acyl Homoserine LactonesJournal of Molecular Biology, 2006
- Construction of Escherichia coli K‐12 in‐frame, single‐gene knockout mutants: the Keio collectionMolecular Systems Biology, 2006
- Hha, YbaJ, and OmpA regulate Escherichia coli K12 biofilm formation and conjugation plasmids abolish motilityBiotechnology & Bioengineering, 2005
- Quorum quenching enzyme activity is widely conserved in the sera of mammalian speciesFEBS Letters, 2005
- Lessons from DNA microarray analysis: the gene expression profile of biofilmsCurrent Opinion in Microbiology, 2005
- Green and red fluorescent protein vectors for use in biofilm studies of the intrinsically resistant Burkholderia cepacia complexJournal of Microbiological Methods, 2004
- Gene Expression Omnibus: NCBI gene expression and hybridization array data repositoryNucleic Acids Research, 2002
- Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl8 and pUC19 vectorsGene, 1985