Abstract
During the transition from exponential to stationary phase E. coli produces a substantial quantity of the small, aromatic signalling molecule indole. In LB medium the supernatant indole concentration reaches a maximum of 0.5–1 mM. At this concentration indole has been implicated in many processes inducing acid resistance and the modulation of virulence. It has recently been shown that cell-associated indole transiently reaches a very high concentration (approx. 60 mM) during stationary phase entry, presumably because indole is being produced more rapidly than it can leave the cell. It is proposed that this indole pulse inhibits growth and cell division, causing the culture to enter stationary phase before nutrients are completely exhausted, with benefits for survival in long-term stationary phase. This study asks how E. coli cells rapidly upregulate indole production during stationary phase entry and why the indole pulse has a duration of only 10–15 min. We find that at the start of the pulse tryptophanase synthesis is triggered by glucose depletion and that this is correlates with the up-regulation of indole synthesis. The magnitude and duration of the resulting indole pulse are dependent upon the availability of exogenous tryptophan. Indole production stops when all the available tryptophan is depleted and the cell-associated indole equilibrates with the supernatant.
Highlights
Indole is a small aromatic molecule produced by over 85 species of bacteria and implicated in multiple signalling processes [1]
Increased tryptophanase expression correlates with the indole pulse We investigated whether increased tryptophanase expression during the approach to stationary phase might be responsible for the initiation of the indole pulse
Our results suggest a simple mechanism for regulation of the cell-associated indole pulse during E. coli stationary phase entry
Summary
Indole is a small aromatic molecule produced by over 85 species of bacteria and implicated in multiple signalling processes [1]. Studies of indole signalling in E. coli have focused primarily on the effect of low (0.5–1 mM), persistent levels of indole, similar to those that are detected in an E. coli LB culture supernatant in stationary phase. At these concentrations indole has a variety of effects including modulation of biofilm formation, virulence and stress responses [2,3,4]. 4–5 mM indole added exogenously to an E. coli culture has been shown reversibly to inhibit growth and cell division [5]. Inhibition of cell division results from indole acting as a proton ionophore [6], reducing the PLOS ONE | DOI:10.1371/journal.pone.0136691 September 2, 2015
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