Abstract
BackgroundMany Gram-positive and Gram-negative bacteria produce large quantities of indole as an intercellular signal in microbial communities. Indole demonstrated to affect gene expression in Escherichia coli as an intra-species signaling molecule. In contrast to E. coli, Salmonella does not produce indole because it does not harbor tnaA, which encodes the enzyme responsible for tryptophan metabolism. Our previous study demonstrated that E. coli-conditioned medium and indole induce expression of the AcrAB multidrug efflux pump in Salmonella enterica serovar Typhimurium for inter-species communication; however, the global effect of indole on genes in Salmonella remains unknown.ResultsTo understand the complete picture of genes regulated by indole, we performed DNA microarray analysis of genes in the S. enterica serovar Typhimurium strain ATCC 14028s affected by indole. Predicted Salmonella phenotypes affected by indole based on the microarray data were also examined in this study. Indole induced expression of genes related to efflux-mediated multidrug resistance, including ramA and acrAB, and repressed those related to host cell invasion encoded in the Salmonella pathogenicity island 1, and flagella production. Reduction of invasive activity and motility of Salmonella by indole was also observed phenotypically.ConclusionOur results suggest that indole is an important signaling molecule for inter-species communication to control drug resistance and virulence of S. enterica.
Highlights
Many Gram-positive and Gram-negative bacteria produce large quantities of indole as an intercellular signal in microbial communities
We demonstrated that an E. coli-conditioned medium and indole induced expression of the acrAB–tolC multidrug efflux system of Salmonella in a RamA regulatordependent manner [35]
Bacterial strains and growth conditions S. enterica serovar Typhimurium strains used in this study were the wild-type strain ATCC14028s [42] and its derivatives
Summary
Many Gram-positive and Gram-negative bacteria produce large quantities of indole as an intercellular signal in microbial communities. Indole demonstrated to affect gene expression in Escherichia coli as an intra-species signaling molecule. In Gram-negative bacteria, these signals could be N-acyl derivatives of homoserine lactone, cyclic dipeptides, and quinolones [6,7,8,9,10,11,12]. Recent studies have revealed that indole is an extracellular signal in E. coli, since it has been demonstrated to regulate uptake, synthesis, and degradation of amino acids in the stationary phase of planktonic cells [31], multicopy plasmid maintenance, cell division [32], biofilm formation [28], acid resistance [33], and expression of multidrug exporters in E. coli [34,35,36] as well as to regulate the pathogenicity island, including the locus of enterocyte effacement of pathogenic E. coli [37,38]. Indole has been demonstrated as an important cell-signaling molecule for a population-based antibiotic resistance mechanism [39]
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