Indole at low concentration helps exponentially growing Escherichia coli survive at high temperature.

Junyan Liu,David Summers,Finbarr Hayes

doi:10.1371/journal.pone.0188853

Abstract

A culture of stationary phase Escherichia coli cells has been reported to produce copious indole when exposed to high temperature (50°C), and this response has been proposed to aid survival. We reinvestigated this phenomenon and found that indole production under these conditions is probably not a direct response to heat stress. Rather, E. coli produces indole when growth is prevented, irrespective of whether this is due to heat stress, antibiotic treatment or the removal of nutrients. Moreover, 300μM indole produced at 50°C does not improve the viability of heat stressed cells. Interestingly, a much lower concentration of indole (20 μM) improves the survival of an indole-negative strain (ΔtnaA) when heat stressed during exponential growth. In addition we have shown that the distribution of tryptophanase, the enzyme responsible for indole synthesis, is highly heterogeneous among cells in a population, except during the transition between exponential and stationary phases. The observation that, despite the presence of the tryptophanase, very little indole is produced during early exponential phase suggests that there is post-translational regulation of the enzyme.

Highlights

Indole was discovered over one hundred years ago and has long been a signature metabolite in the diagnosis of Escherichia coli infection [1]
If indole production is an integral part of the cellular response to heat stress, both tryptophan import and the indole production enzyme (TnaA) must, of necessity, be active at the relevant temperature
Our assay for indole production was based on the observation that stationary phase E. coli in LB broth at 37 ̊C synthesize indole rapidly when the culture medium is supplemented with tryptophan [31]

Summary

Introduction

Indole was discovered over one hundred years ago and has long been a signature metabolite in the diagnosis of Escherichia coli infection [1]. In E. coli indole is produced from tryptophan by the enzyme tryptophanase (TnaA), generating pyruvate and ammonia in the same reaction [2]. Tryptophanase is encoded by the tnaCAB operon that is regulated by catabolite repression [3] and transcription anti-termination [4, 5]. Transcription of the tryptophanase operon initiates from a CAP-dependent promoter which is activated as cAMP builds up [3]. The progression of transcription into the structural gene region requires the presence of exogenous tryptophan, detected by a tnaC-dependent mechanism, to stop Rho-dependent termination before RNA polymerase reaches tnaA and tnaB [6, 7]. The stationary phase sigma factor, σS (rpoS), is essential for normal expression of TnaA [8] and another transcription factor, MarA, can increase TnaA expression [9]

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