EnterohemorrhagicEscherichia coliBiofilms Are Inhibited by 7-Hydroxyindole and Stimulated by Isatin

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Abstract
Since indole is present at up to 500 μM in the stationary phase and is an interspecies biofilm signal (J. Lee, A. Jayaraman, and T. K. Wood, BMC Microbiol. 7:42, 2007), we investigated hydroxyindoles as biofilm signals and found them also to be nontoxic interspecies biofilm signals for enterohemorrhagicEscherichia coliO157:H7 (EHEC),E. coliK-12, andPseudomonas aeruginosa. The genetic basis of EHEC biofilm formation was also explored, and notably, virulence genes in biofilm cells were repressed compared to those in planktonic cells. In Luria-Bertani medium (LB) on polystyrene with quiescent conditions, 7-hydroxyindole decreased EHEC biofilm formation 27-fold and decreased K-12 biofilm formation 8-fold without affecting the growth of planktonic cells. 5-Hydroxyindole also decreased biofilm formation 11-fold for EHEC and 6-fold for K-12. In contrast, isatin (indole-2,3-dione) increased biofilm formation fourfold for EHEC, while it had no effect for K-12. When continuous-flow chambers were used, confocal microscopy revealed that EHEC biofilm formation was reduced 6-fold by indole and 10-fold by 7-hydroxyindole in LB. Whole-transcriptome analysis revealed that isatin represses indole synthesis by repressingtnaABC7- to 37-fold in EHEC, and extracellular indole levels were found to be 20-fold lower. Furthermore, isatin repressed the AI-2 transporterslsrABCDFGKR, while significantly inducing the flagellar genesflgABCDEFGHIJKandfliAEFGILMNOPQ(which led to a 50% increase in motility). 7-Hydroxyindole induces the biofilm inhibitor/stress regulatorycfRand repressescysADIJPU/fliC(which led to a 50% reduction in motility) andpurBCDEFHKLMNRT. Isogenic mutants showed that 7-hydroxyindole inhibitsE. colibiofilm through cysteine metabolism. 7-Hydroxyindole (500 μM) also stimulatesP. aeruginosaPAO1 biofilm formation twofold; therefore, hydroxyindoles are interspecies bacterial signals, and 7-hydroxyindole is a potent EHEC biofilm inhibitor.

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