Indole Transport across Escherichia coli Membranes

Abstract

Indole has many, diverse roles in bacterial signaling. It regulates the transition from exponential to stationary phase, it is involved in the control of plasmid stability, and it influences biofilm formation, virulence, and stress responses (including antibiotic resistance). Its role is not restricted to bacteria, and recently it has been shown to include mutually beneficial signaling between enteric bacteria and their mammalian hosts. In many respects indole behaves like the signaling component of a quorum-sensing system. Indole synthesized within the producer bacterium is exported into the surroundings where its accumulation is detected by sensitive cells. A view often repeated in the literature is that in Escherichia coli the AcrEF-TolC and Mtr transporter proteins are involved in the export and import, respectively, of indole. However, the evidence for their involvement is indirect, and it has been known for a long time that indole can pass directly through a lipid bilayer. We have combined in vivo and in vitro approaches to examine the relative importance of proteinmediated transport and direct passage across the E. coli membrane. We conclude that the movement of indole across the E. coli membrane under normal physiological conditions is independent of AcrEF-TolC and Mtr. Furthermore, direct observation of individual liposomes shows that indole can rapidly cross an E. coli lipid membrane without the aid of any proteinaceous transporter. These observations not only enhance our understanding of indole signaling in bacteria but also provide a simple explanation for the ability of indole to signal between biological kingdoms.

Reduction of Cellular Stress by TolC-Dependent Efflux Pumps in Escherichia coli Indicated by BaeSR and CpxARP Activation of spy in Efflux Mutants

“…Indole induction of spy occurs primarily via BaeRS (24), induction of acrD and mdtABC via BaeRS and CpxARP, and induction of mdtEF via GadX (49). Indole has been reported to be excreted by the AcrEFTolC pump (50), although others have reported that acrEF is not required for indole export (51). Therefore, we tested the effects on spy expression of exposure to various indole concentrations in wild-type (M5402) and tolC mutant (M5403) cells.…”

The Acyl Homoserine Lactone Receptor, SdiA, of Escherichia coli and Salmonella enterica Serovar Typhimurium Does Not Respond to Indole

“…Indole is an intermediate product in tryptophan biosynthesis and is produced by the tryptophan degradation enzyme, tryptophanase (TnaA). Similar to AHLs, indole has been shown to be freely diffusible across bacterial membranes (14,26). While E. coli encodes TnaA and produces indole, S. Typhimurium does not.…”

Novel ATP-driven Pathway of Glycolipid Export Involving TolC Protein

“…S1-S4. 1 To whom correspondence should be addressed: Dept. of Microbiology/Organismic Interactions, Auf der Morgenstelle 28, 72076 Tübingen, Germany.…”

“…Efflux pumps are widespread among Gram-negative bacteria and mediate the secretion of various proteins and a wide variety of other molecules (1)(2)(3)(4)(5). They bridge the periplasm, allowing a one-step transfer of substrates beyond the outer membrane.…”