title: Indole inhibition of N-acylated homoserine lactone-mediated quorum signalling is widespread in Gram-negative bacteria.
abstract: The LuxI/R quorum-sensing system and its associated N-acylated homoserine lactone (AHL) signal is widespread among Gram-negative bacteria. Although inhibition by indole of AHL quorum signalling in Pseudomonas aeruginosa and Acinetobacter oleivorans has been reported previously, it has not been documented among other species. Here, we show that co-culture with wild-type Escherichia coli, but not with E. coli tnaA mutants that lack tryptophanase and as a result do not produce indole, inhibits AHL-regulated pigmentation in Chromobacterium violaceum (violacein), Pseudomonas chlororaphis (phenazine) and Serratia marcescens (prodigiosin). Loss of pigmentation also occurred during pure culture growth of Chro. violaceum, P. chlororaphis and S. marcescens in the presence of physiologically relevant indole concentrations (0.5-1.0 mM). Inhibition of violacein production by indole was counteracted by the addition of the Chro. violaceum cognate autoinducer, N-decanoyl homoserine lactone (C10-HSL), in a dose-dependent manner. The addition of exogenous indole or co-culture with E. coli also affected Chro. violaceum transcription of vioA (violacein pigment production) and chiA (chitinase production), but had no effect on pykF (pyruvate kinase), which is not quorum regulated. Chro. violaceum AHL-regulated elastase and chitinase activity were inhibited by indole, as was motility. Growth of Chro. violaceum was not affected by indole or C10-HSL supplementation. Using a nematode-feeding virulence assay, we observed that survival of Caenorhabditis elegans exposed to Chro. violaceum, P. chlororaphis and S. marcescens was enhanced during indole supplementation. Overall, these studies suggest that indole represents a general inhibitor of AHL-based quorum signalling in Gram-negative bacteria.
authors.affiliation: Department of Biology, Texas State University, 601 University Drive, San Marcos, TX 78666, USA.
authors.forename: Benjamin
authors.initials: B
authors.lastname: Hidalgo-Romano
authors.affiliation: Department of Molecular Biosciences, University of Texas at Austin, Austin, TX 78712, USA.
authors.forename: Jimmy
authors.initials: J
authors.lastname: Gollihar
authors.affiliation: Department of Biology, Southwestern University, Georgetown, TX 78626, USA.
authors.forename: Stacie A
authors.initials: SA
authors.lastname: Brown
authors.affiliation: Department of Molecular Biosciences, University of Texas at Austin, Austin, TX 78712, USA.
authors.forename: Marvin
authors.initials: M
authors.lastname: Whiteley
authors.affiliation: Department of Microbiology and Molecular Genetics, University of Texas Health Science Center at Houston, Houston, TX 77030, USA.
authors.forename: Ernesto
authors.initials: E
authors.lastname: Valenzuela
authors.affiliation: Department of Microbiology and Molecular Genetics, University of Texas Health Science Center at Houston, Houston, TX 77030, USA.
authors.forename: Heidi B
authors.initials: HB
authors.lastname: Kaplan
authors.affiliation: Department of Chemical Engineering, Pennsylvania State University, University Park, PA 16802-4400, USA.
authors.forename: Thomas K
authors.initials: TK
authors.lastname: Wood
authors.affiliation: Department of Biology, Texas State University, 601 University Drive, San Marcos, TX 78666, USA.
authors.forename: Robert J C
authors.initials: RJC
authors.lastname: McLean
mesh_terms: D015107:4-Butyrolactone / Q000031:analogs & derivatives* / Q000378:metabolism; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D002861:Chromobacterium / Q000235:genetics / Q000502:physiology*; D018920:Coculture Techniques; D004926:Escherichia coli / Q000235:genetics / Q000378:metabolism*; D007211:Indoles / Q000378:metabolism*; D011549:Pseudomonas / Q000235:genetics / Q000502:physiology*; D053038:Quorum Sensing; D012706:Serratia marcescens / Q000235:genetics / Q000502:physiology*
chemical_list: D001426:Bacterial Proteins; D007211:Indoles; C088386:homoserine lactone; C030374:indole; D015107:4-Butyrolactone